Dynamic modulation of myelination in response to visual stimuli alters optic nerve conduction velocity

Journal of Neuroscience

Volumn 36, Issue 26, 2016, Pages 6937-6948

  Etxeberria, Ainhoa ^a   Hokanson, Kenton C ^a,b   Dao, Dang Q ^a   Mayoral, Sonia R ^a   Mei, Feng ^a   Redmond, Stephanie A ^a,b   Ullian, Erik M ^a,b   Chan, Jonah R ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Conduction velocity; Glutamate; Monocular deprivation; Myelin; Oligodendrocyte; Optic nerve

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGICAL PROCEDURES; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; MOUSE; MYELINATION; NERVE CONDUCTION VELOCITY; NONHUMAN; OLIGODENDROGLIA; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; VISUAL DEPRIVATION; VISUAL STIMULATION; AGE; ANIMAL; C57BL MOUSE; CYTOLOGY; GENETICS; GENICULATE BODY; METABOLISM; MONOCULAR VISION; MYELIN SHEATH; MYELINATED NERVE; NERVE CONDUCTION; NEWBORN; OPTIC NERVE; ORGANOGENESIS; PHOTOSTIMULATION; PHYSIOLOGY; RETINA GANGLION CELL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; ULTRASTRUCTURE; VISUAL SYSTEM;

ANTIGEN; CHOLERA TOXIN; CHONDROITIN SULFATE PROTEOGLYCAN 4; INSULIN GENE ENHANCER BINDING PROTEIN ISL-1; LIM HOMEODOMAIN PROTEIN; PROTEOGLYCAN; SLC17A6 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; VESICULAR GLUTAMATE TRANSPORTER 2;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; ANTIGENS; CHOLERA TOXIN; GENICULATE BODIES; LIM-HOMEODOMAIN PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURAL CONDUCTION; OPTIC NERVE; ORGANOGENESIS; PHOTIC STIMULATION; PROTEOGLYCANS; RETINAL GANGLION CELLS; SYNAPTIC TRANSMISSION; TRANSCRIPTION FACTORS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VISION, MONOCULAR; VISUAL PATHWAYS;

EID: 84976520404     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0908-16.2016     Document Type: Article

References (52)

1. Almeida RG, Lyons DA (2014) On the resemblance of synapse formation and CNS myelination. Neuroscience 276:98-108. CrossRef Medline
2. Barres BA, Raff MC (1993) Proliferation of oligodendrocyte precursor cells depends on electrical activity in axons. Nature 361:258-260. CrossRef Medline
3. Bechler ME, Byrne L, Ffrench-Constant C (2015) CNS myelin sheath lengths are an intrinsic property of oligodendrocytes. Curr Biol 25:2411-2416. CrossRef Medline
4. Chang KJ, Zollinger DR, Susuki K, Sherman DL, Makara MA, Brophy PJ, Cooper EC, Bennett V, Mohler PJ, Rasband MN (2014) Glial ankyrins facilitate paranodal axoglial junction assembly. Nat Neurosci 17:1673-1681. CrossRef Medline
5. Chen C, Regehr WG (2000) Developmental remodeling of the retinogeniculate synapse. Neuron 28:955-966. CrossRef Medline
6. Chong SYC, Rosenberg SS, Fancy SPJ, Zhao C, Shen YA, Hahn AT, McGee AW, Xu X, Zheng B, Zhang LI, Rowitch DH, Franklin RJM, Lu QR, Chan JR (2012) Neurite outgrowth inhibitor Nogo-A establishes spatial segregation and extent of oligodendrocyte myelination. Proc Natl Acad Sci U S A 109:1299-1304. CrossRef Medline
7. Court FA, Sherman DL, Pratt T, Garry EM, Ribchester RR, Cottrell DF, Fleetwood-Walker SM, Brophy PJ (2004) Restricted growth of Schwann cells lacking Cajal bands slows conduction in myelinated nerves. Nature 431:191-195. CrossRef Medline
8. De Biase LM, Nishiyama A, Bergles DE (2010) Excitability and synaptic communication within the oligodendrocyte lineage. J Neurosci 30:3600-3611. CrossRef Medline
9. De Biase LM, Kang SH, Baxi EG, Fukaya M, Pucak ML, Mishina M, Calabresi PA, Bergles DE (2011) NMDA receptor signaling in oligodendrocyte progenitors is not required for oligodendrogenesis and myelination. J Neurosci 31:12650-12662. CrossRef Medline
10. Demerens C, Stankoff B, Logak M, Anglade P, Allinquant B, Couraud F, Zalc B, Lubetzki C (1996) Induction of myelination in the central nervous system by electrical activity. Proc Natl Acad Sci USA 93:9887-9892. CrossRef
11. + channels. J Neurophysiol 87:1376-1385. Medline
12. Fannon J, Tarmier W, Fulton D (2015) Neuronal activity and AMPA-type glutamate receptor activation regulates the morphological development of oligodendrocyte precursor cells. Glia 63:1021-1035. CrossRef Medline
13. Fukui Y, Hayasaka S, Bedi KS, Ozaki HS, Takeuchi Y (1991) Quantitative study of the development of the optic nerve in rats reared in the dark during early postnatal life. J Anat 174:37-47. Medline
14. + channel block. J Neurosci 16:2659-2670. Medline
15. Gao E, DeAngelis GC, Burkhalter A (2010) Parallel input channels to mouse primary visual cortex. J Neurosci 30:5912-5926. CrossRef Medline
16. Gibson EM, Purger D, Mount CW, Goldstein AK, Lin GL, Wood LS, Inema I, Miller SE, Bieri G, Zuchero JB, Barres BA, Woo PJ, Vogel H, Monje M (2014) Neuronal activity promotes oligodendrogenesis and adaptive myelination in the mammalian brain. Science 344:6183. CrossRef Medline
17. Gudz TI, Komuro H, Macklin WB (2006) Glutamate stimulates oligodendrocyte progenitor migration mediated via an alphav integrin/myelin proteolipid protein complex. J Neurosci 26:2458-2466. CrossRef Medline
18. Guo F, Maeda Y, Ko EM, Delgado M, Horiuchi M, Soulika A, Miers L, Burns T, Itoh T, Shen H, Lee E, Sohn J, Pleasure D (2012) Disruption of NMDA receptors in oligodendroglial lineage cells does not alter their susceptibility to experimental autoimmune encephalomyelitis or their normal development. J Neurosci 32:639-645. CrossRef Medline
19. Hill RA, Patel KD, Goncalves CM, Grutzendler J, Nishiyama A (2014) Modulation of oligodendrocyte generation during a critical temporal window after NG2 cell division. Nat Neurosci 17:1518-1527. CrossRef Medline
20. Hines JH, Ravanelli AM, Schwindt R, Scott EK, Appel B (2015) Neuronal activity biases axon selection for myelination in vivo. Nat Neurosci 18: 683-689. CrossRef Medline
21. Hnasko TS, Chuhma N, Zhang H, Goh GY, Sulzer D, Palmiter RD, Rayport S, and Edwards RH (2010) Vesicular glutamate transport promotes dopamine storage and glutamate corelease in vivo. Neuron 65:643-656. CrossRef Medline
22. Ibrahim M, Butt AM, Berry M (1995) Relationship between myelin sheath diameter and internodal length in axons of the anterior medullary velum of the adult rat. J Neurol Sci 133:119-127. CrossRef Medline
23. Káradóttir R, Cavelier P, Bergersen LH, Attwell D (2005) NMDA receptors are expressed in oligodendrocytes and activated in ischaemia. Nature 438: 1162-1166. CrossRef Medline
24. Koch SM, Dela Cruz CG, Hnasko TS, Edwards RH, Huberman AD, Ullian EM (2011) Pathway-specific genetic attenuation of glutamate release alters select features of competition-based visual circuit refinement. Neuron 71:235-242. CrossRef Medline
25. Kukley M, Capetillo-Zarate E, Dietrich D (2007) Vesicular glutamate release from axons in white matter. Nat Neurosci 10:311-320. CrossRef Medline
26. Lasiene J, Shupe L, Perlmutter S, Horner P (2008) No evidence for chronic demyelination in spared axons after spinal cord injury in a mouse. J Neurosci 28:3887-3896. CrossRef Medline
27. Lee S, Leach MK, Redmond SA, Chong SY, Mellon SH, Tuck SJ, Feng ZQ, Corey JM, Chan JR (2012) A culture system to study oligodendrocyte myelination processes using engineered nanofibers. Nat Methods 9:917-922. CrossRef Medline
28. Linden ML, Heynen AJ, Haslinger RH & Bear MF (2009) Thalamic activity that drives visual cortical plasticity. Nat Neurosci 12:390-392. CrossRef Medline
29. Liu J, Dietz K, DeLoyht JM, Pedre X, Kelkar D, Kaur J, Vialou V, Lobo MK, Dietz DM, Nestler EJ, Dupree J, Casaccia P (2012) Impaired adult myelination in the prefrontal cortex of socially isolated mice. Nat Neurosci 15:1621-1623. CrossRef Medline
30. Lundgaard I, Luzhynskaya A, Stockley JH, Wang Z, Evans KA, Swire M, Volbracht K, Gautier HO, Franklin RJ, Attwell D, Káradóttir RT (2013) Neuregulin and BDNF induce a switch to NMDA receptor-dependent myelination by oligodendrocytes. PLoS Biol 11:e1001743. CrossRef Medline
31. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Palmiter RD, Hawrylycz MJ, Jones AR, et al. (2010) A robust and highthroughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci 13:133-140. CrossRef Medline
32. Maffei A, Nataraj K, Nelson SB, Turrigiano GG (2006) Potentiation of cortical inhibition by visual deprivation. Nature 443:81-84. CrossRef Medline
33. Makinodan M, Rosen KM, Ito S, Corfas G (2012) A critical period for social experience-dependent oligodendrocyte maturation and myelination. Science 337:1357-1360. CrossRef Medline
34. Mangin JM, Gallo V (2011) The curious case of NG2 cells: transient trend or game changer? ASN Neuro 3:e00052. Medline
35. Mangin JM, Kunze A, Chittajallu R, Gallo V (2008) SatelliteNG2progenitor cells share common glutamatergic inputs with associated interneurons in the mouse dentate gyrus. J Neurosci 28:7610-7623. CrossRef Medline
36. McKenzie IA, Ohayon D, Li H, Paes de Faria JP, Emery B, Tohyama K, Richardson WD (2014) Motor skill learning requires active central myelination. Science 346:318-322. CrossRef Medline
37. Mensch S, Baraban M, Almeida R, Czopka T, Ausborn J, El Manira A, Lyons DA (2015) Synaptic vesicle release regulates myelin sheath number of individual oligodendrocytes in vivo. Nat Neurosci 18:628-630. CrossRef Medline
38. Moore CL, Kalil R, Richards W (1976) Development of myelination in optic tract of the cat. J Comp Neurol 165:125-136. CrossRef Medline
39. Perrot R, Lonchampt P, Peterson AC, Eyer J (2007) Axonal neurofilaments control multiple fiber properties but do not influence structure or spacing of nodes of Ranvier. J Neurosci 27:9573-9584. CrossRef Medline
40. Rosenberg SS, Kelland EE, Tokar E, De la Torre AR, Chan JR (2008) The geometric and spatial constraints of the microenvironment induce oligodendrocyte differentiation. Proc Natl Acad Sci U S A 105:14662-14667. CrossRef Medline
41. Rushton WA (1951) A theory of the effects of fibre size in medullated nerve. J Physiol 115:101-122. CrossRef Medline
42. Simpson AH, Gillingwater TH, Anderson H, Cottrell D, Sherman DL, Ribchester RR, Brophy PJ (2013) Effect of limb lengthening on internodal length and conduction velocity of peripheral nerve. J Neurosci 33:4536-4539. CrossRef Medline
43. Srinivas S, Watanabe T, Lin CS, William CM, Tanabe, Y, Jessell TM, Costantini F (2001) Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev Biol 1:4. CrossRef
44. Tauber H, Waehneldt TV, Neuhoff V (1980) Myelination in rabbit optic nerves is accelerated by artificial eye opening. Neurosci Lett 16:235-238. CrossRef Medline
45. Tomassy GS, Berger DR, Chen HH, Kasthuri N, Hayworth KJ, Vercelli A, Seung HS, Lichtman JW and Arlotta P (2014) Distinct profiles of myelin distribution along single axons of pyramidal neurons in the neocortex. Science 344:319-324. CrossRef Medline
46. Turner JP, Salt TE (1998) Characterization of sensory and corticothalamic excitatory. J Physiol 510 3:829-843. CrossRef Medline
47. Wake H, Lee PR, Fields RD (2011) Control of local protein synthesis and initial events in myelination by action potentials. Science 333:1647-1651. CrossRef Medline
48. Wake H, Ortiz FC, Woo DH, Lee PR, Angulo MC, Fields RD (2015) Nonsynaptic junctions on myelinating glia promote preferential myelination of electrically active axons. Nat Commun 6:7844. CrossRef Medline
49. Wu LM, Williams A, Delaney A, Sherman DL, Brophy PJ (2012) Increasing internodal distance in myelinated nerves accelerates nerve conduction to a flat maximum. Curr Biol 22:1957-1961. CrossRef Medline
50. Young KM, Psachoulia K, Tripathi RB, Dunn SJ, Cossell L, Attwell D, Tohyama K, Richardson WD (2013) Oligodendrocyte dynamics in the healthy adult CNS: evidence for myelin remodeling. Neuron 77:873-885. CrossRef Medline
51. Yuan X, Eisen AM, McBain CJ, Gallo V (1998) A role for glutamate and its receptors in the regulation of oligodendrocyte development in cerebellar tissue slices. Development 125:2901-2914. Medline
52. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE (2007) Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10:321-330. CrossRef Medline