Combination of Mn2+enhanced and diffusion tensor MR imaging gives complementary information about injury and regeneration in the adult rat optic nerve

Journal of Magnetic Resonance Imaging

Volumn 29, Issue 1, 2009, Pages 39-51

  Thuen, Marte ^a   Olsen, Øystein ^a   Berry, Martin ^b   Pedersen, Tina Bugge ^a   Kristoffersen, Anders ^c   Haraldseth, Olav ^a,c   Sandvig, Axel ^a   Brekken, Christian ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

Author keywords

DTI; Injury; Manganese; MEMRI; Optic nerve; Regeneration

Indexed keywords

BUPRENORPHINE; MANGANESE CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANISOTROPY; ARTICLE; AXONAL INJURY; CELL SURVIVAL; CONTRAST ENHANCEMENT; CONTROLLED STUDY; CRUSH TRAUMA; DIFFUSION; DIFFUSION TENSOR IMAGING; FEMALE; FISCHER 344 RAT; HISTOPATHOLOGY; NERVE FIBER; NERVE GRAFT; NERVE REGENERATION; NEUROTOXICITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OPTIC NERVE INJURY; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

ANIMALS; CHLORIDES; CONTRAST MEDIA; DIFFUSE AXONAL INJURY; DIFFUSION MAGNETIC RESONANCE IMAGING; FEMALE; IMAGE ENHANCEMENT; MANGANESE COMPOUNDS; NERVE REGENERATION; OPTIC NERVE INJURIES; RATS; RATS, INBRED F344; REPRODUCIBILITY OF RESULTS; RETINAL GANGLION CELLS; SENSITIVITY AND SPECIFICITY;

EID: 60349104038     PISSN: 10531807     EISSN: 15222586     Source Type: Journal    
DOI: 10.1002/jmri.21606     Document Type: Article

References (52)

1. Davies SJA, Fitch MT, Memberg SP, Hall AK, Raisman G, Silver J. Regeneration of adult axons in white matter tracts of the central nervous system. Nature 1997;390:680-683.
2. Ramon y Cajal S. In: DeFelipe J, Jones EG, editors. Degeneration and regeneration of the nervous system. London: Oxford University Press; 1928. p 976.
3. David S, Lacroix S. Molecular approaches to spinal cord repair. Annu Rev Neurosci 2003;26:411-440.
4. Sandvig A, Berry M, Barrett LB, Butt A, Logan A. Myelin-, reactive glia-, and scar-derived CNS axon growth inhibitors: expression, receptor signaling, and correlation with axon regeneration. Glia 2004;46:225-251.
5. Berry M, Carlile J, Hunter A, Tsang W-L, Rosustrel P, Sievers J. Optic nerve regeneration after intravitreal peripheral nerve implants: trajectories of axons regrowing through the optic chiasm into the optic tracts. J Neurocytol 1999;28:721-741.
6. Moon LDF, Asher A, Rhodes KE, Fawcett W. Regeneration of CNS axons back to their target following treatment of adult rat brain with chondroitinase ABC. Nat Neurosci 2001;4:465-466.
7. Li Y, Sauvé Y, Li D, Lund RD, Raisman G. Transplanted olfactory ensheathing cells promote regeneration of cut adult rat optic nerveaxons. J Neurosci 2003;27:7783-7788.
8. Parr AM, Tator CH, Keating A. Bone marrow-derived mesenchymal stromal cells for the repair of central nervous system injury. Bone Marrow Transplant 2003;40:606-619.
9. David S, Aguayo AJ. Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats.Science 1981;214:931-933.
10. Fukunda Y, Watanabe M, Sawai H, Miyoshi T. Functional recovery of vision in regenerated optic nerve fibers. Vision Res 1998;38:1545-1553.
11. Berry M, Charlile J, Hunter A. Peripheral nerve explants grafted into the vitreous body of the eye promote the regeneration of retinal ganglion cell axons severed in the optic nerve. J Neurocytol 1996;25:147-170.
12. Norgren RB, Lehman MN. Herpes simplex virus as a transneuralt racer. Neurosci Biobehav Rev 1998;22:695-708.
13. Paques M, Genevois O, Regnier A, et al. Axon-tracing properties of indocyanine green. Arch Ophthalmol 2003;121:367-370.
14. Reiner A, Veenman CL, Medina L, Jiao Y, Del Mar N, Honig MG. Pathway tracing using biotinylated dextran amines. J Neurosci Methods 2000;103:23-37.
15. Mendonca-Dias MH, Gaggelli E, Lauterbur PC. Paramagnetic contrast agents in nuclear magnetic resonance medical imaging. Se-min Nucl Med 1983;13:364-376.
16. Narita K, Kawasaki F, Kita H. Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res 1990;510:289-295.
17. Pautler RG, Koretsky AP. Tracing odor-induced activation in the olfactory bulbs of mice using manganese-enhanced magnetic resonance imaging. Neuroimage 2002;16:441-448.
18. Takeda A, Kodama Y, Ishiwatari S, Okada S. Manganese transport in the neural circuit ofrat CNS. Brain Res Bull 1998; 45:149-152.
19. Pautler RG, Silva AC, Koretsky AP. In vivo neuronal tract tracing using manganese-enhanced magnetic resonance imaging. Magn Reson Med 1998;40:740-748.
20. 2+-induced contrast. Magn Reson Med 2001;46:424-429.
21. 2. Neuroimage 2004;22:860-867.
22. Van der Linden A, Van Meir V, Tindemans I, Verhoye M, Balthazart J. Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to image brain plasticity in song birds. NMR Biomed 2004;17:602-612.
23. Thuen M, Singstad TE, Bugge Pedersen T, et al. Manganese-enhanced MRI of the optic visual pathway and optic nerve injury in adult rats. J Magn Reson Imaging 2005;22:492-500.
24. Aschner M, Erikson KM, Dorman DC. Manganese dosimetry: species differences and implications for neurotoxicity. Crit Rev Toxicol 2005;35:1-32.
25. Bearer EL, Falzone TL, Zhang XW, Biris O, Rasin A, Jacobs RE. Role of neuronal activity and kinesin on tract tracing by manganese-enhanced MRI (MEMRI). Neuroimage 2007;37:S37-S46.
26. Beaulieu C. The basis of anisotropic water diffusion in the nervous system-a technical review. NMR Biomed 2002;15:435-455.
27. Le Biham D, Mangin J-F, Poupon C, et al. Diffusion tensor imaging: concepts and applications. J Magn Reson Imaging 2001;13:534-546.
28. Sun S-W, Liang H-F, Cross AH, Song S-K. Evolving Wallerian degeneration after transient retinal ischemia in mice characterized by diffusion tensor imaging. Neuroimage 2008;40:1-10.
29. Olsen ø, Thuen M, Berry M, et al. Axon tracing in the adult rat optic nerve and tract after intravitreal injection of MnDPDP using a semi-automatic segmentation technique. J Magn Reson Imaging 2008;27:34-42.
30. Firbank MJ, Coulthard A, Harrison RM, Williams ED. A comparison of two methods for measuring the signal to noise ratio on MR images. Phys Med Biol 1999;44:N261-N264.
31. Kristoffersen A. Optimal estimation of the diffusion coefficient from non-averaged and averaged noisy magnitude data. J Magn Reson 2007;187:293-305.
32. Leon S, Yin Y, Nguyen J, Irwin N, Benowitz LI. Lens injury stimulates axon regeneration in the mature rat optic nerve. J Neurosci 2000;20:4615-4626.
33. Isenmann S, Kretz A, Cellerino A. Molecular determinants ofretinal ganglion cell development, survival, and regeneration. Prog Retinal Eye Res 2003;22:483-543.
34. Heumann R. Regulation of the synthesis of nerve growth factor. J Exp Biol 1987;132:133-150.
35. Lindsey JD, Scadeng M, Dubowitz DJ, Crowston JG, Weinreb RN. Magnetic resonance imaging of the visual system in vivo: transsyn-aptic illumination of V1 and V2 visual cortex. Neuroimage 2007;34:1619-1626.
36. 2+ ho-meostasis in the gerbil hippocampus following brief transient ischemia. Brain Res 1986;364:372-376.
37. Garbossa D, Fontanella M, Fronda C, et al. New strategies for repairing the injured spinal cord: the role of stem cells. Neurol Res 2006;28:500-504.
38. Archibald FS, Fridovich I. The scavenging of superoxide radical by manganese complexes: in vitro. Arch Biochem Biophys 1982;214: 452-463.
39. Brurok H, Ardenkjcer-Larsen JH, Hansson G, et al. Manganese dipyridoxyl diphosphate: MRI contrast agent with antioxidative and cardioprotective properties? Biochem Biophys Res Commun 1999;254:768-772.
40. Bernstein MA, King KF, Zhou XJ, editors. Echo train pulse sequences. Handbook of MRI pulse sequences. Burlington, VT:Elsevier Academic Press; 2004. p 702-801.
41. Wheeler-Kingshott CAM, Trip SA, Symms MR, Parker GJM, Barker GJ, Miller DH. In vivo diffusion tensor imaging of the human optic nerve: pilot study in normal controls. Magn Reson Med 2006;56:446-451.
42. Jones DK. The effect of gradient sampling schemes on measures derived from diffusion tensor MRI: a Monte Carlo study. Magn Reson Med 2004;51:807-815.
43. Tekk̈ov SB, Brown AM, Ransom BR. Axon function persists during anoxia in mammalian white matter. J Cereb Blood Flow Metab 2003;23:1340-1347.
44. Sun S-W, Liang H-F, Le TQ, Armstrong RC, Cross AH, Song S-K. Differential sensitivity of in vivo and ex vivo diffusion tensor imaging to evolving optic nerve injury in mice with retinal ischemia. Neuroimage 2006;32:1195-1204.
45. Song S-K, Sun S-W, Ramsbottom MJ, Chang C, Russen J, Cross AH. Dysmyelination revealed through MRI as increased radial (but unenhanced axial) diffusion of water. Neuroimage 2002;17:1429-1436.
46. Wu Q, Butzkueven H, Gresle M, et al. MR diffusion changes correlation with ultra-structurally defined axonal degeneration in mu-rine optic nerve. Neuroimage 2007;37:1138-1147.
47. Gullapalli J, Krejza J, SchwartzED. In vivo DTI evaluation of white matter tracts in rat spinal cord. J Magn Reson Imaging 2006;24:231-234.
48. Stieltjes B, Klussmann S, Bock M, et al. Manganese-enhanced magnetic resonance imaging for in vivo assessment of damage and functional improvement following spinal cord injury in mice. Magn Reson Med 2006; 55:1124-1131.
49. Song S-K, Sun S-W, Ju W-K, Lin S-J, Cross AH, Neufeld AH. Diffusion tensor imaging detects and differentiates axon and mye-lin degeneration in mouse optic nerve after retinal ischemia. Neu-roimage 2003;20:1714-1722.
50. Thomalla G, Glauche V, Koch MA, Beaulieu C, Weiller C, Röther J.Diffusion tensor imaging detects early Wallerian degeneration of the pyramidal tract after ischemic stroke. Neuroimage 2004;22:1767-1774.
51. Heemskerk AM, Strijkers GM, Drost MR, van Bochove GS, Nicolay K. Skeletal muscle degeneration and regeneration after femoral artery ligation in mice: monitoring with diffusion MR imaging. Ra-diology2007;243:413-421.
52. Chuang K-H, Koretsky A. Improved neuronal tract tracing using manganese enhanced magnetic resonance imaging with fast T1 mapping. Magn Reson Med 2006;55:604-611.