Home LiteratureArticle Details
PMID: 12533611 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Correlation between brain reorganization, ischemic damage, and neurologic status after transient focal cerebral ischemia in rats: a functional magnetic resonance imaging study.

Dijkhuizen RM, Singhal AB, Mandeville JB, Wu O, Halpern EF, Finklestein SP, Rosen BR, Lo EH

Abstract

The pattern and role of brain plasticity in stroke recovery has been incompletely characterized. Both ipsilesional and contralesional changes have been described, but it remains unclear how these relate to functional recovery. Our goal was to correlate brain activation patterns with tissue damage, hemodynamics, and neurologic status after temporary stroke, using functional magnetic resonance imaging (fMRI). Transverse relaxation time (T2)-weighted, diffusion-weighted, and perfusion MRI were performed at days 1 (n = 7), 3 (n = 7), and 14 (n = 7) after 2 hr unilateral middle cerebral artery occlusion in rats. Functional activation and cerebrovascular reactivity maps were generated from contrast-enhanced fMRI during forelimb stimulation and hypercapnia, respectively. Before MRI, rats were examined neurologically. We detected loss of activation responses in the ipsilesional sensorimotor cortex, which was related to T2 lesion size (r = -0.858 on day 3, r = -0.979 on day 14; p < 0.05). Significant activation responses in the contralesional hemisphere were detected at days 1 and 3. The degree of shift in balance of activation between the ipsilesional and contralesional hemispheres, characterized by the laterality index, was linked to the T2 and apparent diffusion coefficient in the ipsilesional contralesional forelimb region of the primary somatosensory cortex and primary motor cortex at day 1 (r = -0.807 and 0.782, respectively; p < 0.05) and day 14 (r = -0.898 and -0.970, respectively; p < 0.05). There was no correlation between activation parameters and perfusion status or cerebrovascular reactivity. Finally, we found that the laterality index and neurologic status changed in parallel over time after stroke, so that when all time points were grouped together, neurologic status was inversely correlated with the laterality index (r = -0.571; p = 0.016). This study suggests that the degree of shift of activation balance toward the contralesional hemisphere early after stroke increases with the extent of tissue injury and that functional recovery is associated mainly with preservation or restoration of activation in the ipsilesional hemisphere.

MeSH Terms
Animals Behavior, Animal Brain/blood supply,pathology,physiopathology Diffusion Magnetic Resonance Imaging Disease Models, Animal Forelimb/innervation,physiopathology Functional Laterality Hemodynamics Hypercapnia/physiopathology Infarction, Middle Cerebral Artery/complications,pathology,physiopathology Ischemic Attack, Transient/complications,pathology,physiopathology Magnetic Resonance Angiography Magnetic Resonance Imaging Male Neurologic Examination Neuronal Plasticity Rats Rats, Sprague-Dawley Recovery of Function Severity of Illness Index Water/metabolism
Chemicals
Water
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Dijkhuizen Rick M
Athinoula A. Martinos Center for Biomedical Imaging, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, USA. rick@invivonmr.uu.nl
Singhal Aneesh B
Mandeville Joseph B
Wu Ona
Halpern Elkan F
Finklestein Seth P
Rosen Bruce R
Lo Eng H
References (47)
47 references, click to expand
  1. Changes in GABA(A) and GABA(B) receptor binding following cortical photothrombosis: a quantitative receptor autoradiographic study.
    Neuroscience. 1999;93(4):1233-40 PMID: 10501447
  2. Widespread up-regulation of N-methyl-D-aspartate receptors after focal photothrombotic lesion in rat brain.
    Neurosci Lett. 1999 Oct 1;273(2):77-80 PMID: 10505620
  3. Cortical plasticity after stroke: implications for rehabilitation.
    Rev Neurol (Paris). 1999;155(9):713-7 PMID: 10528355
  4. Bihemispheric contribution to motor recovery after stroke: A longitudinal study with transcranial doppler ultrasonography.
    Cerebrovasc Dis. 1999 Nov-Dec;9(6):337-44 PMID: 10545692
  5. Evolution of functional reorganization in hemiplegic stroke: a serial positron emission tomographic activation study.
    Ann Neurol. 1999 Dec;46(6):901-9 PMID: 10589543
  6. Brain plasticity and stroke rehabilitation. The Willis lecture.
    Stroke. 2000 Jan;31(1):223-30 PMID: 10625741
  7. Mapping clinically relevant plasticity after stroke.
    Neuropharmacology. 2000 Mar 3;39(5):842-51 PMID: 10699449
  8. Evolution of cortical activation during recovery from corticospinal tract infarction.
    Stroke. 2000 Mar;31(3):656-61 PMID: 10700500
  9. Treatment-induced cortical reorganization after stroke in humans.
    Stroke. 2000 Jun;31(6):1210-6 PMID: 10835434
  10. Functional differentiation of multiple perilesional zones after focal cerebral ischemia.
    J Cereb Blood Flow Metab. 2000 Aug;20(8):1149-65 PMID: 10950376
  11. Cytoprotection does not preserve brain functionality in rats during the acute post-stroke phase despite evidence of non-infarction provided by MRI.
    NMR Biomed. 2000 Oct;13(6):361-70 PMID: 11002315
  12. Neuromagnetic integrated methods tracking human brain mechanisms of sensorimotor areas 'plastic' reorganisation.
    Brain Res Brain Res Rev. 2000 Sep;33(2-3):131-54 PMID: 11011062
  13. Functional imaging correlates of recovery after stroke in humans.
    J Cereb Blood Flow Metab. 2000 Dec;20(12):1619-31 PMID: 11129778
  14. Long-term deficits following cerebral hypoxia-ischemia in four-week-old rats: correspondence between behavioral, histological, and magnetic resonance imaging assessments.
    Exp Neurol. 2001 Feb;167(2):272-81 PMID: 11161615
  15. Functional recovery after brain lesion--contralateral neuromodulation: an fMRI study.
    Neuroreport. 2001 May 25;12(7):1543-7 PMID: 11388445
  16. T2-weighted MRI correlates with long-term histopathology, neurology scores, and skilled motor behavior in a rat stroke model.
    Ann N Y Acad Sci. 2001 Jun;939:283-96 PMID: 11462782
  17. Functional magnetic resonance imaging of reorganization in rat brain after stroke.
    Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12766-71 PMID: 11606760
  18. Plasticity of the human motor cortex and recovery from stroke.
    Brain Res Brain Res Rev. 2001 Oct;36(2-3):169-74 PMID: 11690613
  19. Dynamics of motor network overactivation after striatocapsular stroke: a longitudinal PET study using a fixed-performance paradigm.
    Stroke. 2001 Nov;32(11):2534-42 PMID: 11692013
  20. Application of magnetic resonance to animal models of cerebral ischemia.
    J Magn Reson Imaging. 2001 Nov;14(5):491-509 PMID: 11747001
  21. Functional reorganization of motor cortex increases with greater axonal injury from CADASIL.
    Stroke. 2002 Feb;33(2):502-8 PMID: 11823660
  22. Investigation of mechanisms underlying transient T2 normalization in longitudinal studies of ischemic stroke.
    J Magn Reson Imaging. 2002 Feb;15(2):130-6 PMID: 11836767
  23. Recovery of motor and language abilities after stroke: the contribution of functional imaging.
    Prog Neurobiol. 2002 Feb;66(2):109-22 PMID: 11900884
  24. Application of magnetic resonance imaging to the measurement of neurodegeneration in rat brain: MRI data correlate strongly with histology and enzymatic analysis.
    Magn Reson Imaging. 1992;10(5):773-8 PMID: 1361020
  25. Overgrowth and pruning of dendrites in adult rats recovering from neocortical damage.
    Brain Res. 1992 May 22;581(1):156-60 PMID: 1498666
  26. Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy.
    Magn Reson Med. 1990 May;14(2):330-46 PMID: 2345513
  27. Reversible middle cerebral artery occlusion without craniectomy in rats.
    Stroke. 1989 Jan;20(1):84-91 PMID: 2643202
  28. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination.
    Stroke. 1986 May-Jun;17(3):472-6 PMID: 3715945
  29. Neocortical neural sprouting, synaptogenesis, and behavioral recovery after neocortical infarction in rats.
    Stroke. 1995 Nov;26(11):2135-44 PMID: 7482662
  30. Role of vasogenic edema and tissue cavitation in ischemic evolution on diffusion-weighted imaging: comparison with multiparameter MR and immunohistochemistry.
    AJNR Am J Neuroradiol. 1995 May;16(5):1107-15 PMID: 7639135
  31. Comparison of diffusion-weighted MRI with changes in cell volume in a rat model of brain injury.
    NMR Biomed. 1994 Mar;7(1-2):96-100 PMID: 8068532
  32. Water diffusion and acute stroke.
    Magn Reson Med. 1994 Feb;31(2):154-63 PMID: 8133751
  33. Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging and light and electron microscopic study.
    Radiology. 1993 Nov;189(2):439-48 PMID: 8210373
  34. Mechanisms underlying functional recovery following stroke.
    Can J Neurol Sci. 1995 Nov;22(4):257-63 PMID: 8599767
  35. Continuous assessment of relative cerebral blood volume in transient ischemia using steady state susceptibility-contrast MRI.
    Magn Reson Med. 1996 Feb;35(2):168-73 PMID: 8622580
  36. Synaptogenesis and dendritic growth in the cortex opposite unilateral sensorimotor cortex damage in adult rats: a quantitative electron microscopic examination.
    Brain Res. 1996 Sep 9;733(1):142-8 PMID: 8891261
  37. High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis.
    Magn Reson Med. 1996 Nov;36(5):715-25 PMID: 8916022
  38. Spreading of vasogenic edema and cytotoxic edema assessed by quantitative diffusion and T2 magnetic resonance imaging.
    Stroke. 1997 Feb;28(2):419-26; discussion 426-7 PMID: 9040700
  39. Recovery and repair issues after stroke from the scientific perspective.
    Curr Opin Neurol. 1997 Feb;10(1):49-51 PMID: 9099527
  40. Intracisternal basic fibroblast growth factor enhances functional recovery and up-regulates the expression of a molecular marker of neuronal sprouting following focal cerebral infarction.
    Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):8179-84 PMID: 9223335
  41. Reorganization of motor output in the non-affected hemisphere after stroke.
    Brain. 1997 Sep;120 ( Pt 9):1579-86 PMID: 9313641
  42. Behavioral, anatomical, and physiological aspects of recovery of motor function following stroke.
    Brain Res Brain Res Rev. 1997 Sep 30;25(1):125-32 PMID: 9370054
  43. Dynamic functional imaging of relative cerebral blood volume during rat forepaw stimulation.
    Magn Reson Med. 1998 Apr;39(4):615-24 PMID: 9543424
  44. Early impairment and late recovery of synaptic transmission in the rat dentate gyrus following transient forebrain ischemia in vivo.
    Brain Res. 1998 Jul 13;799(1):130-7 PMID: 9666102
  45. Mechanisms of motor dysfunction after transient MCA occlusion: persistent transmission failure in cortical synapses is a major determinant.
    Stroke. 1998 Sep;29(9):1988-93; discussion 1994 PMID: 9731628
  46. Neural activation of the brain with hemodynamic insufficiency.
    J Cereb Blood Flow Metab. 1998 Sep;18(9):960-7 PMID: 9740099
  47. Imaging recovery from stroke.
    Exp Brain Res. 1998 Nov;123(1-2):13-7 PMID: 9835387
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-01-15
Pages
510-7
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6741861
Subset
IM
Grants
NINDS NIH HHS · R01-NS38731 · United States
NCI NIH HHS · P01-CA48729 · United States
NINDS NIH HHS · P50 NS010828 · United States
NHLBI NIH HHS · R01 HL039810 · United States
NINDS NIH HHS · R01 NS038477 · United States
NHLBI NIH HHS · R01-HL39810 · United States
NCRR NIH HHS · P41 RR014075 · United States
NCRR NIH HHS · P41-RR14075 · United States
NINDS NIH HHS · R01-NS37074 · United States
NINDS NIH HHS · P50-NS10828 · United States
NINDS NIH HHS · R01-NS38477 · United States
NINDS NIH HHS · R01 NS037074 · United States
NINDS NIH HHS · R01 NS038731 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com