Mossy fiber sprouting in pilocarpine-induced status epilepticus rat hippocampus: A correlative study of diffusion spectrum imaging and histology

NeuroImage

Volumn 41, Issue 3, 2008, Pages 789-800

  Kuo, Li Wei ^a   Lee, Chun Yao ^b   Chen, Jyh Horng ^a   Wedeen, Van Jay ^d   Chen, Chih Chuan ^c   Liou, Horng Huei ^b,c   Tseng, Wen Yih Isaac ^b,c  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Anisotropy; Diffusion MRI; Diffusion spectrum imaging; Diffusivity; Hippocampus; Mossy fiber sprouting; Temporal lobe epilepsy

Indexed keywords

PILOCARPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANISOTROPY; ARTICLE; CELL HETEROGENEITY; CONTROLLED STUDY; CORRELATION ANALYSIS; DIFFUSION ANISOTROPY; DIFFUSION WEIGHTED IMAGING; DISEASE SEVERITY; EPILEPTIC FOCUS; EPILEPTIC STATE; FOLLOW UP; HIPPOCAMPUS; HISTOPATHOLOGY; IMAGE RECONSTRUCTION; LONGITUDINAL STUDY; MALE; MOSSY FIBER; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RAT; STAINING; TEMPORAL LOBE EPILEPSY;

ANIMALS; ANISOTROPY; DIFFUSION MAGNETIC RESONANCE IMAGING; IMAGING, THREE-DIMENSIONAL; MALE; MOSSY FIBERS, HIPPOCAMPAL; MUSCARINIC ANTAGONISTS; PILOCARPINE; RATS; RATS, WISTAR; STATUS EPILEPTICUS;

EID: 44449155694     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2008.03.013     Document Type: Article

References (56)

1. Basser P.J. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 8 (1995) 333-344
2. Bito Y., Hirata S., and Yamamoto E. Optimal gradient factors for ADC measurements. Proc. Int. Soc. Magn. Reson. Med. ISMRM, California (1995) 913
3. Buckmaster P.S., and Dudek F.E. Neuron loss, granule cell axon reorganization, and functional changes in the dentate gyrus of epileptic kainate-treated rats. J. Comp. Neurol. 385 (1997) 385-404
4. Callaghan P.T. Principles of nuclear magnetic resonance microscopy (1991), Clarendon Press, Oxford
5. Chang B.S., and Lowenstein D.H. Epilepsy. N. Engl. J. Med. 349 (2003) 1257-1266
6. Chiang W.Y., Wedeen V.J., Kuo L.W., Peng M.H., and Tseng W.Y. Diffusion spectrum imaging using Body-Center-Cubic sampling scheme. Proc. Int. Soc. Magn. Reson. Med. ISMRM, California (2006) 1041
7. Cilio M.R., Sogawa Y., Cha B.H., Liu X., Huang L.T., and Holmes G.L. Long-term effects of status epilepticus in the immature brain are specific for age and model. Epilepsia 44 (2003) 518-528
8. Claiborne B.J., Rea M.A., and Terrian D.M. Detection of zinc in isolated nerve terminals using a modified Timm's sulfide-silver method. J. Neurosci. Methods 30 (1989) 17-22
9. Cronin J., and Dudek F.E. Chronic seizures and collateral sprouting of dentate mossy fibers after kainic acid treatment in rats. Brain Res. 474 (1988) 181-184
10. Danscher G. Histochemical demonstration of heavy metals. A revised version of the sulphide silver method suitable for both light and electronmicroscopy. Histochemistry 71 (1981) 1-16
11. Duc C.O., Trabesinger A.H., Weber O.M., Meier D., Walder M., Wieser H.G., and Boesiger P. Quantitative 1H MRS in the evaluation of mesial temporal lobe epilepsy in vivo. Magn. Reson. Imaging 16 (1998) 969-979
12. Duncan J.S. Neuroimaging methods to evaluate the etiology and consequences of epilepsy. Epilepsy Res. 50 (2002) 131-140
13. Duncan J.S. Epilepsy surgery. Clin. Med. 7 (2007) 137-142
14. Duncan J.S., Sander J.W., Sisodiya S.M., and Walker M.C. Adult epilepsy. Lancet 367 (2006) 1087-1100
15. Fabene P.F., Marzola P., Sbarbati A., and Bentivoglio M. Magnetic resonance imaging of changes elicited by status epilepticus in the rat brain: diffusion-weighted and T2-weighted images, regional blood volume maps, and direct correlation with tissue and cell damage. NeuroImage 18 (2003) 375-389
16. Franck J.E., Pokorny J., Kunkel D.D., and Schwartzkroin P.A. Physiologic and morphologic characteristics of granule cell circuitry in human epileptic hippocampus. Epilepsia 36 (1995) 543-558
17. Gilbert R.J., Magnusson L.H., Napadow V.J., Benner T., Wang R., and Wedeen V.J. Mapping complex myoarchitecture in the bovine tongue with diffusion-spectrum magnetic resonance imaging. Biophys. J. 91 (2006) 1014-1022
18. Gilbert R.J., Wedeen V.J., Magnusson L.H., Benner T., Wang R., Dai G., Napadow V.J., and Roche K.K. Three-dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography. Anat. Rec., A. Discov. Mol. Cell. Evol. Biol. 288 (2006) 1173-1182
19. Jaermann T., Crelier G., Pruessmann K.P., Golay X., Netsch T., van Muiswinkel A.M., Mori S., van Zijl P.C., Valavanis A., Kollias S., and Boesiger P. SENSE-DTI at 3 T. Magn. Reson. Med. 51 (2004) 230-236
20. Jones D.K., and Basser P.J. "Squashing peanuts and smashing pumpkins": how noise distorts diffusion-weighted MR data. Magn. Reson. Med. 52 (2004) 979-993
21. Jones D.K., Horsfield M.A., and Simmons A. Optimal strategies for measuring diffusion in anisotropic systems by magnetic resonance imaging. Magn. Reson. Med. 42 (1999) 515-525
22. Kim J.A., Koyama R., Yamada R.X., Yamada M.K., Nishiyama N., Matsuki N., and Ikegaya Y. Environmental control of the survival and differentiation of dentate granule neurons. Cereb. Cortex 14 (2004) 1358-1364
23. Kimiwada T., Juhasz C., Makki M., Muzik O., Chugani D.C., Asano E., and Chugani H.T. Hippocampal and thalamic diffusion abnormalities in children with temporal lobe epilepsy. Epilepsia 47 (2006) 167-175
24. Kurian M., Spinelli L., Delavelle J., Willi J.P., Velazquez M., Chaves V., Habre W., Meagher-Villemure K., Roulet E., Villeneuve J.G., and Seeck M. Multimodality imaging for focus localization in pediatric pharmacoresistant epilepsy. Epileptic Disord. 9 (2007) 20-31
25. Le Bihan D., Poupon C., Amadon A., and Lethimonnier F. Artifacts and pitfalls in diffusion MRI. J. Magn. Reson. Imaging 24 (2006) 478-488
26. Lin C.P., Tseng W.Y., Weng J.C., Wedeen V.J., and Chen J.H. Reduced encoding of diffusion spectrum imaging with cross-term correction. Proceedings of the 1st IEEE EMBS Conference on Neural Engineering, Capri Island, Italy (2003) 561-563
27. Lin C.P., Wedeen V.J., Chen J.H., Yao C., and Tseng W.Y. Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms. NeuroImage 19 (2003) 482-495
28. Liu Z., Yang Y., Silveira D.C., Sarkisian M.R., Tandon P., Huang L.T., Stafstrom C.E., and Holmes G.L. Consequences of recurrent seizures during early brain development. Neuroscience 92 (1999) 1443-1454
29. Mello L.E., Cavalheiro E.A., Tan A.M., Kupfer W.R., Pretorius J.K., Babb T.L., and Finch D.M. Circuit mechanisms of seizures in the pilocarpine model of chronic epilepsy: cell loss and mossy fiber sprouting. Epilepsia 34 (1993) 985-995
30. Mori S., and van Zijl P.C. A motion correction scheme by twin-echo navigation for diffusion-weighted magnetic resonance imaging with multiple RF echo acquisition. Magn. Reson. Med. 40 (1998) 511-516
31. Nadler J.V. The recurrent mossy fiber pathway of the epileptic brain. Neurochem. Res. 28 (2003) 1649-1658
32. Nairismagi J., Grohn O.H., Kettunen M.I., Nissinen J., Kauppinen R.A., and Pitkanen A. Progression of brain damage after status epilepticus and its association with epileptogenesis: a quantitative MRI study in a rat model of temporal lobe epilepsy. Epilepsia 45 (2004) 1024-1034
33. Nairismagi J., Pitkanen A., Narkilahti S., Huttunen J., Kauppinen R.A., and Grohn O.H. Manganese-enhanced magnetic resonance imaging of mossy fiber plasticity in vivo. NeuroImage 30 (2006) 130-135
34. Obenaus A., and Jacobs R.E. Magnetic resonance imaging of functional anatomy: use for small animal epilepsy models. Epilepsia 48 Suppl. 4 (2007) 11-17
35. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1996), Academic Press
36. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Clin. Neurophysiol. 32 (1972) 281-294
37. Reese T.G., Heid O., Weisskoff R.M., and Wedeen V.J. Reduction of eddy-current-induced distortion in diffusion MRI using a twice-refocused spin echo. Magn. Reson. Med. 49 (2003) 177-182
38. Reese T.G., Benner T., Wang R., Feinberg D.A., and Wedeen V.J. Halving imaging time of whole brain diffusion spectrum imaging (DSI) by using simultaneous echo refocusing (SER) EPI. Proceedings of the 14th Meeting of the International Society for Magnetic Resonance in Medicine, Seattle, USA (2006) 1044
39. Rugg-Gunn F.J., Eriksson S.H., Symms M.R., Barker G.J., and Duncan J.S. Diffusion tensor imaging of cryptogenic and acquired partial epilepsies. Brain 124 (2001) 627-636
40. Salmenpera T.M., Simister R.J., Bartlett P., Symms M.R., Boulby P.A., Free S.L., Barker G.J., and Duncan J.S. High-resolution diffusion tensor imaging of the hippocampus in temporal lobe epilepsy. Epilepsy Res. 71 (2006) 102-106
41. Scharfman H.E. The CA3 "backprojection" to the dentate gyrus. Prog. Brain Res. 163 (2007) 627-637
42. Scharfman H.E., Goodman J.H., and Sollas A.L. Granule-like neurons at the hilar/CA3 border after status epilepticus and their synchrony with area CA3 pyramidal cells: functional implications of seizure-induced neurogenesis. J. Neurosci. 20 (2000) 6144-6158
43. Scharfman H.E., Sollas A.L., Smith K.L., Jackson M.B., and Goodman J.H. Structural and functional asymmetry in the normal and epileptic rat dentate gyrus. J. Comp. Neurol. 454 (2002) 424-439
44. Shepherd T.M., Ozarslan E., King M.A., Mareci T.H., and Blackband S.J. Structural insights from high-resolution diffusion tensor imaging and tractography of the isolated rat hippocampus. NeuroImage 32 (2006) 1499-1509
45. Shepherd T.M., Wirth III E.D., Thelwall P.E., Chen H.X., Roper S.N., and Blackband S.J. Water diffusion measurements in perfused human hippocampal slices undergoing tonicity changes. Magn. Reson. Med. 49 (2003) 856-863
46. Siddiqui A.H., and Joseph S.A. CA3 axonal sprouting in kainate-induced chronic epilepsy. Brain Res. 1066 (2005) 129-146
47. Stringer J.L., Williamson J.M., and Lothman E.W. Induction of paroxysmal discharges in the dentate gyrus: frequency dependence and relationship to afterdischarge production. J. Neurophysiol. 62 (1989) 126-135
48. Sutula T. Seizure-induced axonal sprouting: assessing connections between injury, local circuits, and epileptogenesis. Epilepsy Curr. 2 (2002) 86-91
49. Sutula T., Cascino G., Cavazos J., Parada I., and Ramirez L. Mossy fiber synaptic reorganization in the epileptic human temporal lobe. Ann. Neurol. 26 (1989) 321-330
50. Thivard L., Lehericy S., Krainik A., Adam C., Dormont D., Chiras J., Baulac M., and Dupont S. Diffusion tensor imaging in medial temporal lobe epilepsy with hippocampal sclerosis. NeuroImage 28 (2005) 682-690
51. Tseng W.Y., Lin C.P., Chen J.H., and Wedeen V.J. Diffusion spectrum imaging of complex cortical cytoarchitecture in adult rats. Proceedings of the 10th Meeting of the International Society for Magnetic Resonance in Medicine, Hawaii, USA (2002) 441
52. van Eijsden P., Notenboom R.G., Wu O., de Graan P.N., van Nieuwenhuizen O., Nicolay K., and Braun K.P. In vivo 1H magnetic resonance spectroscopy, T2-weighted and diffusion-weighted MRI during lithium-pilocarpine-induced status epilepticus in the rat. Brain Res. 1030 (2004) 11-18
53. Wall C.J., Kendall E.J., and Obenaus A. Rapid alterations in diffusion-weighted images with anatomic correlates in a rodent model of status epilepticus. AJNR Am. J. Neuroradiol. 21 (2000) 1841-1852
54. Wedeen V.J., Hagmann P., Tseng W.Y., Reese T.G., and Weisskoff R.M. Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn. Reson. Med. 54 (2005) 1377-1386
55. Weih K.S., Driesel W., von Mengershausen M., and Norris D.G. Online motion correction for diffusion-weighted segmented-EPI and FLASH imaging. Magma 16 (2004) 277-283
56. Williams P.A., Wuarin J.P., Dou P., Ferraro D.J., and Dudek F.E. Reassessment of the effects of cycloheximide on mossy fiber sprouting and epileptogenesis in the pilocarpine model of temporal lobe epilepsy. J. Neurophysiol. 88 (2002) 2075-2087