Functional magnetic resonance imaging of rats with experimental autoimmune encephalomyelitis reveals brain cortex remodeling

Journal of Neuroscience

Volumn 35, Issue 27, 2015, Pages 10088-10100

  Tambalo, Stefano ^a,b   Peruzzotti Jametti, Luca ^c   Rigolio, Roberta ^d   Fiorini, Silvia ^a   Bontempi, Pietro ^a   Mallucci, Giulia ^c,e   Balzarotti, Beatrice ^c   Marmiroli, Paola ^d   Sbarbati, Andrea ^a   Cavaletti, Guido ^d   Pluchino, Stefano ^c   Marzola, Pasquina ^a,b  

^a UNIVERSITY OF VERONA   (Italy)

^b National Interuniversity Consortium of Materials Science and Technology INSTM UdR Pisa   (Italy)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF MILANO BICOCCA   (Italy)

^e UNIVERSITY OF PAVIA   (Italy)

Author keywords

Cortical reorganization; Experimental autoimmune encephalomyelitis; Functional magnetic resonance imaging; Multiple sclerosis; Neuroimmunology; Rain plasticity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY TEMPERATURE; BRAIN ATROPHY; BREATHING RATE; CORPUS CALLOSUM; DENDRITIC SPINE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRAY MATTER; MALE; MULTIPLE SCLEROSIS; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR CORTEX; SOMATOSENSORY STIMULATION; VOXEL BASED MORPHOMETRY; WHITE MATTER; ANIMAL; BLOOD; BRAIN CORTEX; DENDRITE; DISEASE MODEL; ELECTROSTIMULATION; HINDLIMB; IMAGE PROCESSING; INNERVATION; METABOLISM; NERVE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOLOGY; PHYSIOLOGY; SENSORY NERVE; ULTRASTRUCTURE; VASCULARIZATION;

CYTOKINE; NERVE PROTEIN; OXYGEN;

AFFERENT PATHWAYS; ANIMALS; CEREBRAL CORTEX; CORPUS CALLOSUM; CYTOKINES; DENDRITES; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; HINDLIMB; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NERVE TISSUE PROTEINS; NEURONS; OXYGEN; RATS;

EID: 84936864771     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0540-15.2015     Document Type: Article

References (59)

1. Andres RH, Horie N, Slikker W, Keren-Gill H, Zhan K, Sun G, Manley NC, Pereira MP, Sheikh LA, McMillan EL, Schaar BT, Svendsen CN, Bliss TM, Steinberg GK (2011) Human neural stem cells enhance structural plasticity and axonal transport in the ischaemic brain. Brain 134: 1777-1789. CrossRef Medline.
2. Ashburner J, Friston KJ (2000) Voxel-based morphometry-the methods. Neuroimage 11: 805-821. CrossRef Medline.
3. Bacigaluppi M, Pluchino S, Peruzzotti-Jametti L, Kilic E, Kilic U, Salani G, Brambilla E, West MJ, Comi G, Martino G, Hermann DM (2009) Delayed post-ischaemic neuroprotection following systemic neural stem cell transplantation involves multiple mechanisms. Brain 132: 2239-2251. CrossRef Medline.
4. Badovinac V, Mostarica-Stojković M, Dinarello CA, Stosić-Grujicić S (1998) Interleukin-1 receptor antagonist suppresses experimental autoimmune encephalomyelitis (EAE) in rats by influencing the activation and proliferation of encephalitogenic cells. J Neuroimmunol 85: 87-95. CrossRef Medline.
5. Benedict RH, Bruce JM, Dwyer MG, Abdelrahman N, Hussein S, Weinstock-Guttman B, Garg N, Munschauer F, Zivadinov R (2006) Neocortical atrophy, third ventricular width, and cognitive dysfunction in multiple sclerosis. Arch Neurol 63: 1301-1306. CrossRef Medline.
6. Buckle GJ (2005) Functional magnetic resonance imaging and multiple sclerosis: the evidence for neuronal plasticity. J Neuroimaging 15: 82S-93S. CrossRef Medline.
7. Calautti C, Naccarato M, Jones PS, Sharma N, Day DD, Carpenter AT, Bullmore ET, Warburton EA, Baron JC (2007) The relationship between motor deficit and hemisphere activation balance after stroke: a 3T fMRI study. Neuroimage 34: 322-331. CrossRef Medline.
8. Ceccarelli A, Rocca MA, Valsasina P, Rodegher M, Falini A, Comi G, FilippiM (2010) Structural and functional magnetic resonance imaging correlates of motor network dysfunction in primary progressive multiple sclerosis. Eur J Neurosci 31: 1273-1280. CrossRef Medline.
9. Cerasa A, Fera F, Gioia MC, Liguori M, Passamonti L, Nicoletti G, Vercillo L, Paolillo A, Clodomiro A, Valentino P, Quattrone A (2006) Adaptive cortical changes and the functional correlates of visuo-motor integration in relapsing-remitting multiple sclerosis. Brain Res Bull 69: 597-605. CrossRef Medline.
10. Chard DT, Griffin CM, Parker GJ, Kapoor R, Thompson AJ, Miller DH (2002) Brain atrophy in clinically early relapsing-remitting multiple sclerosis. Brain 125: 327-337. CrossRef Medline.
11. Comi G, Rocca MA, Filippi M (2004) Brain plasticity in multiple sclerosis. Eur Neurol 51: 189-190. CrossRef Medline.
12. Dijkhuizen RM, Ren J, Mandeville JB, Wu O, Ozdag FM, Moskowitz MA, Rosen BR, Finklestein SP (2001) Functional magnetic resonance imaging of reorganization in rat brain after stroke. Proc Natl Acad Sci U S A 98: 12766-12771. CrossRef Medline.
13. Dimitrijević M, Rauski A, Radojević K, Kosec D, Stanojević S, Pilipović I, Leposavić G (2007) Beta-adrenoceptor blockade ameliorates the clinical course of experimental allergic encephalomyelitis and diminishes its aggravation in adrenalectomized rats. Eur J Pharmacol 577: 170-182. CrossRef Medline.
14. Douaud G, Smith S, Jenkinson M, Behrens T, Johansen-Berg H, Vickers J, James S, Voets N, Watkins K, Matthews PM, James A (2007) Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain 130: 2375-2386. CrossRef Medline.
15. Filippi M, Rocca MA (2004) Cortical reorganisation in patients with MS. J Neurol Neurosurg Psychiatry 75: 1087-1089. CrossRef Medline.
16. Filippi M, Rocca MA (2009) Functional MR imaging in multiple sclerosis. Neuroimaging Clin N Am 19: 59-70. CrossRef Medline.
17. Filippi M, Rocca MA (2013) Multiple sclerosis: linking disability and spinal cord imaging outcomes in MS. Nat Rev Neurol 9: 189-190. CrossRef Medline.
18. Filippi M, Rocca MA, Barkhof F, BrückW, Chen JT, Comi G, DeLuca G, De Stefano N, Erickson BJ, Evangelou N, Fazekas F, Geurts JJ, Lucchinetti C, Miller DH, Pelletier D, Popescu BF, Lassmann H, Attendees of the Correlation between Pathological MRIfiMSw (2012) Association between pathological and MRI findings in multiple sclerosis. Lancet Neurol 11: 349-360. CrossRef Medline.
19. Foster CA, Mechtcheriakova D, Storch MK, Balatoni B, Howard LM, Bornancin F, Wlachos A, Sobanov J, Kinnunen A, BaumrukerT (2009) FTY720 rescue therapy in the dark agouti rat model of experimental autoimmune encephalomyelitis: expression of central nervous system genes and reversal of bloodbrain-barrier damage. Brain Pathol 19: 254-266. CrossRef Medline.
20. Freund P, Weiskopf N, Ward NS, Hutton C, Gall A, Ciccarelli O, Craggs M, Friston K, Thompson AJ (2011) Disability, atrophy and cortical reorganization following spinal cord injury. Brain 134: 1610-1622. CrossRef Medline.
21. Ghosh A, Haiss F, Sydekum E, Schneider R, Gullo M, Wyss MT, Mueggler T, Baltes C, Rudin M, Weber B, Schwab ME (2010) Rewiring of hindlimb corticospinal neurons after spinal cord injury. Nat Neurosci 13: 97-104. CrossRef Medline.
22. Giatti S, Boraso M, Abbiati F, Ballarini E, Calabrese D, Santos-Galindo M, Rigolio R, Pesaresi M, Caruso D, Viviani B, Cavaletti G, Garcia-Segura LM, Melcangi RC (2013) Multimodal analysis in acute and chronic experimental autoimmune encephalomyelitis. J Neuroimmune Pharmacol 8: 238-250. CrossRef Medline.
23. Gozzi A, Agosta F, Massi M, Ciccocioppo R, Bifone A (2013) Reduced limbic metabolism and fronto-cortical volume in rats vulnerable to alcohol addiction. Neuroimage 69: 112-119. CrossRef Medline.
24. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17: 825-841. CrossRef Medline.
25. Johnson GV, Jope RS (1992) The role of microtubule-associated protein 2 (MAP-2) in neuronal growth, plasticity, and degeneration. J Neurosci Res 33: 505-512. CrossRef Medline.
26. Keilholz SD, Silva AC, Raman M, Merkle H, Koretsky AP (2006) BOLD and CBV-weighted functional magnetic resonance imaging of the rat somatosensory system. Magn Reson Med 55: 316-324. CrossRef Medline.
27. Li Q, Cheung C, Wei R, Hui ES, Feldon J, Meyer U, Chung S, Chua SE, Sham PC, Wu EX, McAlonan GM (2009) Prenatal immune challenge is an environmental risk factor for brain and behavior change relevant to schizophrenia: evidence from MRI in a mouse model. PLoS One 4: e6354. CrossRef Medline.
28. Loitfelder M, Fazekas F, Petrovic K, Fuchs S, Ropele S, Wallner-Blazek M, Jehna M, Aspeck E, Khalil M, Schmidt R, Neuper C, Enzinger C (2011) Reorganization in cognitive networks with progression of multiple sclerosis: insights from fMRI. Neurology 76: 526-533. CrossRef Medline.
29. MacKenzie-Graham A, Rinek GA, Avedisian A, Gold SM, Frew AJ, Aguilar C, Lin DR, Umeda E, Voskuhl RR, Alger JR (2012) Cortical atrophy in experimental autoimmune encephalomyelitis: in vivo imaging. Neuroimage 60: 95-104. CrossRef Medline.
30. Marzola P, Sbarbati A (2004) Magnetic resonance imaging in animal models of pathologies. Methods Enzymol 386: 177-200. CrossRef Medline.
31. Nathoo N, Yong VW, Dunn JF (2014) Using magnetic resonance imaging in animal models to guide drug development in multiple sclerosis. Mult Scler 20: 3-11. CrossRef Medline.
32. Nichols TE, Holmes AP (2002) Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 15: 1-25. CrossRef Medline.
33. Pantano P, Iannetti GD, Caramia F, Mainero C, Di Legge S, Bozzao L, Pozzilli C, Lenzi GL (2002) Cortical motor reorganization after a single clinical attack of multiple sclerosis. Brain 125: 1607-1615. CrossRef Medline.
34. Pantano P, Mainero C, Caramia F (2006) Functional brain reorganization in multiple sclerosis: evidence from fMRI studies. J Neuroimaging 16: 104-114. CrossRef Medline.
35. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates: San Diego: Academic.
36. Pelletier J, Suchet L, Witjas T, Habib M, Guttmann CR, Salamon G, Lyon-Caen O, Chérif AA (2001) A longitudinal study of callosal atrophy and interhemispheric dysfunction in relapsing-remitting multiple sclerosis. Arch Neurol 58: 105-111. CrossRef Medline.
37. Ramu J, Bockhorst KH, Grill RJ, Mogatadakala KV, Narayana PA (2007) Cortical reorganization in NT3-treated experimental spinal cord injury: Functional magnetic resonance imaging. Exp Neurol 204: 58-65. CrossRef Medline.
38. Reddy H, Narayanan S, Arnoutelis R, Jenkinson M, Antel J, Matthews PM, Arnold DL (2000) Evidence for adaptive functional changes in the cerebral cortex with axonal injury from multiple sclerosis. Brain 123: 2314-2320. CrossRef Medline.
39. Reddy H, Narayanan S, Woolrich M, Mitsumori T, Lapierre Y, Arnold DL, Matthews PM (2002) Functional brain reorganization for hand movement in patients with multiple sclerosis: defining distinct effects of injury and disability. Brain 125: 2646-2657. CrossRef Medline.
40. Rocca MA, Colombo B, Falini A, Ghezzi A, Martinelli V, Scotti G, Comi G, Filippi M (2005) Cortical adaptation in patients with MS: a crosssectional functional MRI study of disease phenotypes. Lancet Neurol 4: 618-626. CrossRef Medline.
41. Sanfilipo MP, Benedict RH, Sharma J, Weinstock-Guttman B, Bakshi R (2005) The relationship between whole brain volume and disability in multiple sclerosis: a comparison of normalized gray vs. white matter with misclassification correction. Neuroimage 26: 1068-1077. CrossRef Medline.
42. Schnabel JA, Tanner C, Castellano-Smith AD, Degenhard A, Leach MO, Hose DR, Hill DL, Hawkes DJ (2003) Validation of nonrigid image registration using finite-element methods: application to breastMRimages. IEEE Trans Med Imaging 22: 238-247. CrossRef Medline.
43. Schoonheim MM, Filippi M (2012) Functional plasticity in MS: friend or foe? Neurology 79: 1418-1419. CrossRef Medline.
44. Schwarz AJ, Danckaert A, Reese T, Gozzi A, Paxinos G, Watson C, Merlo-Pich EV, Bifone A (2006) A stereotaxic MRI template set for the rat brain with tissue class distribution maps and co-registered anatomical atlas: application to pharmacological MRI. Neuroimage 32: 538-550. CrossRef Medline.
45. Shih YY, Wey HY, De La Garza BH, Duong TQ (2011) Striatal and cortical BOLD, blood flow, blood volume, oxygen consumption, and glucose consumption changes in noxious forepaw electrical stimulation. J Cereb Blood Flow Metab 31: 832-841. CrossRef Medline.
46. Smith SM, JenkinsonM, WoolrichMW, Beckmann CF, Behrens TE, Johansen-Berg H, Bannister PR, De Luca M, Drobnjak I, Flitney DE, Niazy RK, Saunders J, Vickers J, ZhangY, DeStefano N, Brady JM, MatthewsPM (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23 [Suppl 1]: S208-S219. CrossRef.
47. Staiger JF, Flagmeyer I, Schubert D, Zilles K, Kötter R, Luhmann HJ (2004) Functional diversity of layer IV spiny neurons in rat somatosensory cortex: quantitative morphology of electrophysiologically characterized and biocytin labeled cells. Cereb Cortex 14: 690-701. CrossRef Medline.
48. StorchMK, StefferlA, BrehmU, Weissert R, WallströmE, KerschensteinerM, Olsson T, Linington C, LassmannH (1998) Autoimmunityto myelin oligodendrocyte glycoprotein in rats mimics the spectrum of multiple sclerosis pathology. Brain Pathol 8: 681-694. CrossRef Medline.
49. Stosic-Grujicic S, Ramic Z, Bumbasirevic V, Harhaji L, Mostarica-Stojkovic M (2004) Induction of experimental autoimmune encephalomyelitis in Dark Agouti rats without adjuvant. Clin Exp Immunol 136: 49-55. CrossRef Medline.
50. Tambalo S, Daducci A, Fiorini S, Boschi F, Mariani M, Marinone M, Sbarbati A, Marzola P (2009) Experimental protocol for activation-induced manganese-enhanced MRI (AIM-MRI) based on quantitative determination of Mn content in rat brain by fast T1 mapping. Magn Reson Med 62: 1080-1084. CrossRef Medline.
51. Tona F, Petsas N, Sbardella E, Prosperini L, Carmellini M, Pozzilli C, Pantano P (2014) Multiple sclerosis: altered thalamic resting-state functional connectivity and its effect on cognitive function. Radiology 271: 814-821. CrossRef Medline.
52. Van Camp N, Peeters RR, Van der Linden A (2005) A comparison between blood oxygenation level-dependent and cerebral blood volume contrast in the rat cerebral and cerebellar somatosensoric cortex during electrical paw stimulation. J Magn Reson Imaging 22: 483-491. CrossRef Medline.
53. Van Camp N, Verhoye M, Van der Linden A (2006a) Stimulation of the rat somatosensory cortex at different frequencies and pulse widths. NMR Biomed 19: 10-17. CrossRef Medline.
54. Van Camp N, Verhoye M, De Zeeuw CI, Van der Linden A (2006b) Light stimulus frequency dependence of activity in the rat visual system as studied with high-resolution BOLD fMRI. J Neurophysiol 95: 3164-3170. CrossRef Medline.
55. Weber R, Ramos-Cabrer P, Wiedermann D, van Camp N, HoehnM (2006) A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat. Neuroimage 29: 1303-1310. CrossRef Medline.
56. Wegner C, Esiri MM, Chance SA, Palace J, Matthews PM (2006) Neocortical neuronal, synaptic, and glial loss in multiple sclerosis. Neurology 67: 960-967. CrossRef Medline.
57. Zhao F, Welsh D, Williams M, Coimbra A, Urban MO, Hargreaves R, Evelhoch J, Williams DS (2012) fMRI of pain processing in the brain: a within-animal comparative study of BOLD vs. CBV and noxious electrical vs. noxious mechanical stimulation in rat. Neuroimage 59: 1168-1179. CrossRef Medline.
58. Zhao F, Williams M, Bowlby M, Houghton A, Hargreaves R, Evelhoch J, Williams DS (2014) Qualification of fMRI as a biomarker for pain in anesthetized rats by comparison with behavioral response in conscious rats. Neuroimage 84: 724-732. CrossRef Medline.
59. Zhu B, Luo L, Moore GR, Paty DW, Cynader MS (2003) Dendritic and synaptic pathology in experimental autoimmune encephalomyelitis. Am J Pathol 162: 1639-1650. CrossRef Medline.