Early prediction of functional recovery after experimental stroke: Functional magnetic resonance imaging, electrophysiology, and behavioral testing in rats

Journal of Neuroscience

Volumn 28, Issue 5, 2008, Pages 1022-1029

  Weber, Ralph ^a,b   Ramos Cabrer, Pedro ^a,c   Justicia, Carlos ^a,d   Wiedermann, Dirk ^a   Strecker, Cordula ^a   Sprenger, Christiane ^a   Hoehn, Mathias ^a  

^a MAX PLANCK INSTITUTE FOR NEUROLOGICAL RESEARCH   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c Instituto de Salud Carlos III   (Spain)

^d INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

Author keywords

fMRI; Functional recovery; Functional reorganization; Ischemia; Neurovascular coupling; Stroke

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD OXYGENATION; BRAIN DAMAGE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ELECTROPHYSIOLOGY; EVOKED RESPONSE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; RAT; SOMATOSENSORY CORTEX; SOMATOSENSORY SYSTEM; STROKE;

ANIMALS; BEHAVIOR, ANIMAL; ELECTROPHYSIOLOGY; EVOKED POTENTIALS, SOMATOSENSORY; MAGNETIC RESONANCE IMAGING; MALE; PREDICTIVE VALUE OF TESTS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SOMATOSENSORY CORTEX; STROKE; TIME FACTORS;

EID: 38749089033     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4147-07.2008     Document Type: Article

References (41)

1. Abo M, Chen Z, Lai LJ, Reese T, Bjelke B (2001) Functional recovery after brain lesion-contralateral neuromodulation: an fMRI study. NeuroReport 12:1543-1547.
2. Aoyagi A, Saito H, Abe K, Nishiyama N (1998) Early impairment and late recovery of synaptic transmission in the rat dentate gyrus following transient forebrain ischemia in vivo. Brain Res 799:130-137.
3. Arthurs OJ, Williams EJ, Carpenter TA, Pickard JD, Boniface SJ (2000) Linear coupling between functional magnetic resonance imaging and evoked potential amplitude in human somatosensory cortex. Neuroscience 101:803-806.
4. Brinker G, Bock C, Busch E, Krep H, Hossmann KA, Hoehn-Berlage M (1999) Simultaneous recording of evoked potentials and T2*-weighted MR images during somatosensory stimulation of rat. Magn Reson Med 41:469-473.
5. Carey LM, Abbott DF, Puce A, Jackson GD, Syngeniotis A, Donnan GA (2002) Reemergence of activation with poststroke somatosensory recovery: a serial fMRI case study. Neurology 59:749-752.
6. Dijkhuizen RM, Nicolay K (2003) Magnetic resonance imaging in experimental models of brain disorders. J Cereb Blood Flow Metab 23:1383-1402.
7. 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 USA 98:12766-12771.
8. Dijkhuizen RM, Singhal AB, Mandeville JB, Wu O, Halpern EF, Finklestein SP, Rosen BR, Lo EH (2003) Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study. J Neurosci 23:510-517.
9. Eis M, Els T, Hoehn-Berlage M, Hossmann KA (1994) Quantitative diffusion MR imaging of cerebral tumor and edema. Acta Neurochir Suppl (Wien) 60:344-346.
10. Feeney DM, De Smet AM, Rai S (2004) Noradrenergic modulation of hemiplegia: facilitation and maintenance of recovery. Restor Neurol Neurosci 22:175-190.
11. Forman SD, Cohen JD, Fitzgerald M, Eddy WF, Mintun MA, Noll DC (1995) Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn Reson Med 33:636-647.
12. Gsell W, Burke M, Wiedermann D, Bonvento G, Silva AC, Dauphin F, Bührle C, Hoehn M, Schwindt W (2006) Differential effects of NMDA and AMPA glutamate receptors on functional magnetic resonance imaging signals and evoked neuronal activity during forepaw stimulation of the rat. J Neurosci 26:8409-8416.
13. Hedenquist P, Hellebrekers LJ (2003) Laboratory animal analgesia, anesthesia and euthanasia. In: Handbook of laboratory animal science (Hau J, Van Hoosier GLJ, eds), pp 413-455. Boca Raton, FL: CRC.
14. Heeger DJ, Ress D (2002) What does fMRI tell us about neuronal activity? Nat Rev Neurosci 3:142-151.
15. Hossmann KA (1997) Reperfusion of the brain after global ischemia-hemodynamic disturbances. Shock 8:95-101.
16. Kim YR, Huang IJ, Lee SR, Tejima E, Mandeville JB, van Meer MP, Dai G, Choi YW, Dijkhuizen RM, Lo EH, Rosen BR (2005) Measurements of BOLD/CBV ratio show altered fMRI hemodynamics during stroke recovery in rats. J Cereb Blood Flow Metab 25:820-829.
17. Krainik A, Hund-Georgiadis M, Zysset S, von Cramon DY (2005) Regional impairment of cerebrovascular reactivity and BOLD signal in adults after stroke. Stroke 36:1146-1152.
18. Logothetis NK, Wandell BA (2004) Interpreting the BOLD signal. Annu Rev Physiol 66:735-769.
19. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150-157.
20. Longa EZ, Weinstein PR, Carlson S, Cummins R (1989) Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20:84-91.
21. Norup Nielsen A, Lauritzen M (2001) Coupling and uncoupling of activity-dependent increases of neuronal activity and blood flow in rat somatosensory cortex. J Physiol (Lond) 533:773-785.
22. Ogawa S, Lee TM, Stepnoski R, Chen W, Zhu XH, Ugurbil K (2000) An approach to probe some neural systems interaction by functional MRI at neural time scale down to milliseconds. Proc Natl Acad Sci USA 97:11026-11031.
23. Oliviero A, Tecchio F, Zappasodi F, Pasqualetti P, Salustri C, Lupoi D, Ercolani M, Romani GL, Rossini PM (2004) Brain sensorimotor hand area functionality in acute stroke: insights from magnetoencephalography. NeuroImage 23:542-550.
24. Palmer GC, Peeling J, Corbett D, Del Bigio MR, Hudzik TJ (2001) T2-weighted MRi correlates with long-term histopathology, neurology scores, and skilled motor behavior in a rat stroke model. Ann NY Acad Sci 939:283-296.
25. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. San Diego: Academic.
26. Pineiro R, Pendlebury S, Johansen-Berg H, Matthews PM (2002) Altered hemodynamic responses in patients after subcortical stroke measured by functional MRI. Stroke 33:103-109.
27. Ramos-Cabrer P, Weber R, Wiedermann D, Hoehn M (2005) Continuous noninvasive monitoring of transcutaneous blood gases for a stable and persistent BOLD contrast in fMRI studies in the rat. NMR Biomed 18:440-446.
28. Rossini PM, Calautti C, Pauri F, Baron JC (2003) Post-stroke plastic reorganisation in the adult brain. Lancet Neurol 2:493-502.
29. Rossini PM, Altamura C, Ferretti A, Vernieri F, Zappasodi F, Caulo M, Pizzella V, Del Gratta C, Romani GL, Tecchio F (2004) Does cerebrovascular disease affect the coupling between neuronal activity and local haemodynamics? Brain 127:99-110.
30. Sakatani K, Iizuka H, Young W (1990) Somatosensory evoked potentials in rat cerebral cortex before and after middle cerebral artery occlusion. Stroke 21:124-132.
31. Sauter A, Reese T, Porszasz R, Baumann D, Rausch M, Rudin M (2002) Recovery of function in cytoprotected cerebral cortex in rat stroke model assessed by functional MRI. Magn Reson Med 47:759-765.
32. Schallert T, Woodlee M, Fleming SM (2002) Disentangling multiple types of recovery from brain injury. In: Pharmacology of cerebral ischemia (Krieglstein J, Klumpp S, eds), pp 201-216. Stuttgart, Germany: Medpharm.
33. Schmitz B, Bock C, Hoehn-Berlage M, Kerskens CM, Bottiger BW, Hossmann KA (1998) Recovery of the rodent brain after cardiac arrest: a functional MRI study [Erratum (1998) 40:340]. Magn Reson Med 39:783-788.
34. Silverman J, Muir IIIWW (1993) A review of laboratory animal anesthesia with chloral hydrate and chloralose. Lab Anim Sci 43:210-216.
35. Smirnakis SM, Schmidt MC, Weber B, Tolias AS, Augath M, Logothetis NK (2007) Spatial specificity of BOLD versus cerebral blood volume fMRI for mapping cortical organization. J Cereb Blood Flow Metab 27:1248-1261.
36. Strupp JP (1996) Stimulate: a GUI based fMRI analysis software package. NeuroImage 3:S607.
37. Ueki M, Linn F, Hossmann KA (1988) Functional activation of cerebral blood flow and metabolism before and after global ischemia of rat brain. J Cereb Blood Flow Metab 8:486-494.
38. Waltz AG (1969) Red venous blood: occurrence and significance in ischemic and nonischemic cerebral cortex. J Neurosurg 31:141-148.
39. Weber R, Ramos-Cabrer P, Wiedermann D, van Camp N, Hoehn M (2006) A fully noninvasive and robust experimental protocol for longitudinal fMRI studies in the rat. NeuroImage 29:1303-1310.
40. Wegener S, Weber R, Ramos-Cabrer P, Uhlenkueken U, Sprenger C, Wiedermann D, Villringer A, Hoehn M (2006) Temporal profile of T2-weighted MRI distinguishes between pannecrosis and selective neuronal death after transient focal cerebral ischemia in the rat. J Cereb Blood Flow Metab 26:38-47.
41. Wikström H, Roine RO, Aronen HJ, Salonen O, Sinkkonen J, Ilmoniemi RJ, Huttunen J (2000) Specific changes in somatosensory evoked magnetic fields during recovery from sensorimotor stroke. Ann Neurol 47:353-360.