A rat's whiskers point the way toward a novel stimulus-dependent, protective stroke therapy

Neuroscientist

Volumn 19, Issue 3, 2013, Pages 313-328

  Frostig, Ron D ^a,b   Lay, Christopher C ^a,b   Davis, Melissa F ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ischemia; protection; reperfusion; rodent model; stimulation treatment; stroke

Indexed keywords

TRIPHENYLTETRAZOLIUM;

BEHAVIOR CHANGE; BLOOD OXYGENATION; BLOOD PRESSURE; BRAIN BLOOD FLOW; BRAIN CORTEX; BRAIN ELECTROPHYSIOLOGY; BRAIN FUNCTION; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN PROTECTION; BREATHING RATE; COLLATERAL CIRCULATION; EVOKED RESPONSE; EXPLORATORY BEHAVIOR; HEART RATE; HISTOPATHOLOGY; HUMAN; INJURY SEVERITY; MIDDLE CEREBRAL ARTERY OCCLUSION; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SENSORIMOTOR FUNCTION; SENSORY STIMULATION; SOMATOSENSORY CORTEX; STROKE PATIENT; TREATMENT RESPONSE; VIBRISSA; ANIMAL; BRAIN; DISEASE MODEL; INNERVATION; OUTCOME ASSESSMENT; PATHOPHYSIOLOGY; PHYSICAL STIMULATION; PHYSIOLOGY; PROCEDURES; RAT; SENSORY NERVE; STROKE; TIME FACTOR; TREATMENT OUTCOME; VASCULARIZATION;

AFFERENT PATHWAYS; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; HUMANS; OUTCOME ASSESSMENT (HEALTH CARE); PHYSICAL STIMULATION; RATS; STROKE; TIME FACTORS; TREATMENT OUTCOME; VIBRISSAE;

EID: 84877741654     PISSN: 10738584     EISSN: 10894098     Source Type: Journal    
DOI: 10.1177/1073858412462607     Document Type: Review

References (67)

1. Adibhatla RM, Hatcher JF. Lipid oxidation and peroxidation in CNS health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal. 2010 ; 12 (1). 125-69
2. Baron JC. Mapping the ischaemic penumbra with PET: a new approach. Brain. 2001 ; 124 (Pt 1). 2-4
3. Bederson JB, Pitts LH, Tsuji M, Nishimura MC, Davis RL, Bartkowski H. Rat middle cerebral artery occlusion: evaluation of the model and development of a neurologic examination. Stroke. 1986 ; 17 (3). 472-6
4. Blumenfeld H Neuroanatomy through clinical cases. Sunderland, MA: Sinauer Associates ; 2002:
5. Burnett MG, Shimazu T, Szabados T, Muramatsu H, Detre JA, Greenberg JH. Electrical forepaw stimulation during reversible forebrain ischemia decreases infarct volume. Stroke. 2006 ; 37 (5). 1327-31
6. Caplan LR 2009. Caplan's stroke: a clinical approach. 4 ed. Phildelphia: Saunders/Elsevier. Phildelphia: Saunders/Elsevier ; 2009:
7. Carmichael ST. Rodent models of focal stroke: size, mechanism, and purpose. NeuroRx. 2005 ; 2 (3). 396-409
8. Chen ST, Hsu CY, Hogan EL, Maricq H, Balentine JD. A model of focal ischemic stroke in the rat: reproducible extensive cortical infarction. Stroke. 1986 ; 17 (4). 738-43
9. Chen-Bee CH, Agoncillo T, Xiong Y, Frostig RD. The triphasic intrinsic signal: implications for functional imaging. J Neurosci. 2007 ; 27 (17). 4572-86
10. Chiganos TC, Jensen W, Rousche PJ. Electrophysiological response dynamics during focal cortical infarction. J Neural Eng. 2006 ; 3 (4). L15-22
11. Cirstea MC, Levin MF. Compensatory strategies for reaching in stroke. Brain. 2000 ; 123 (Pt 5). 940-53
12. Cook DJ, Teves L, Tymianski M. Treatment of stroke with a PSD-95 inhibitor in the gyrencephalic primate brain. Nature. 2012 ; 483 (7388). 213-7
13. Coyle P. Different susceptibilities to cerebral infarction in spontaneously hypertensive (SHR) and normotensive Sprague-Dawley rats. Stroke. 1986 ; 17 (3). 520-5
14. Coyle P. Spatial relations of dorsal anastomoses and lesion border after middle cerebral artery occlusion. Stroke. 1987 ; 18 (6). 1133-40
15. Crafton KR, Mark AN, Cramer SC. Improved understanding of cortical injury by incorporating measures of functional anatomy. Brain. 2003 ; 126 (Pt 7). 1650-9
16. Cramer SC, Riley JD. Neuroplasticity and brain repair after stroke. Curr Opin Neurol. 2008 ; 21 (1). 76-82
17. Davis MF, Lay CC, Chen-Bee CH, Frostig RD. Amount but not pattern of protective sensory stimulation alters recovery after permanent middle cerebral artery occlusion. Stroke. 2011a ; 42 (3). 792-8
18. Davis MF, Lay CC, Chen-Bee CH, Frostig RD Neuroscience 2011. Washington, DC: Society for Neuroscience ; 2011b:
19. Del Zoppo GJ. Why do all drugs work in animals but none in stroke patients? 1. Drugs promoting cerebral blood flow. J Intern Med. 1995 ; 237 (1). 79-88
20. Del Zoppo GJ, Saver JL, Jauch EC, Adams HP. Expansion of the time window for treatment of acute ischemic stroke with intravenous tissue plasminogen activator: a science advisory from the American Heart Association/American Stroke Association. Stroke. 2009 ; 40 (8). 2945-8
21. DiNapoli VA, Huber JD, Houser K, Li X, Rosen CL. Early disruptions of the blood-brain barrier may contribute to exacerbated neuronal damage and prolonged functional recovery following stroke in aged rats. Neurobiol Aging. 2008 ; 29 (5). 753-64
22. Rodent models of stroke. Dirnagl U, ed. New York: Spring Science+Business Media ; 2010:
23. Dirnagl U, Iadecola C, Moskowitz MA. Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 1999 ; 22 (9). 391-7
24. Dirnagl U, Kaplan B, Jacewicz M, Pulsinelli W. Continuous measurement of cerebral cortical blood flow by laser-Doppler flowmetry in a rat stroke model. J Cereb Blood Flow Metab. 1989 ; 9 (5). 589-96
25. Durukan A, Tatlisumak T. Acute ischemic stroke: overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav. 2007 ; 87 (1). 179-97
26. Frostig RD, Chen-Bee CH In vivo optical imaging of brain function. 2009. Visualizing adult cortical plasticity using intrinsic signal optical imaging. In: FrostigRD, editor. In vivo optical imaging of brain function. 2 ed. Boca Raton, FL: CRC Press. p 255-87. Frostig RD, ed. Boca Raton, FL: CRC Press ; 2009: 255-87.
27. Frostig RD, Lieke EE, Ts'o DY, Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci U S A. 1990 ; 87 (16). 6082-6
28. Ginsberg MD. Life after cerovive: a personal perspective on ischemic neuroprotection in the post-NXY-059 era. Stroke. 2007 ; 38 (6). 1967-72
29. Graham SM, McCullough LD, Murphy SJ. Animal models of ischemic stroke: balancing experimental aims and animal care. Comp Med. 2004 ; 54 (5). 486-96
30. Greenberg DA, Jin K. Regenerating the brain. Int Rev Neurobiol. 2007 ; 77: 1-29
31. Grinvald A, Lieke E, Frostig RD, Gilbert CD, Wiesel TN. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature. 1986 ; 324 (6095). 361-4
32. Grotta J. Why do all drugs work in animals but none in stroke patients? 2. Neuroprotective therapy. J Intern Med. 1995 ; 237 (1). 89-94
33. Hossmann KA. Viability thresholds and the penumbra of focal ischemia. Ann Neurol. 1994 ; 36 (4). 557-65
34. Hoyte L, Kaur J, Buchan AM. Lost in translation: taking neuroprotection from animal models to clinical trials. Exp Neurol. 2004 ; 188 (2). 200-4
35. Iadecola C, Nedergaard M. Glial regulation of the cerebral microvasculature. Nat Neurosci. 2007 ; 10 (11). 1369-76
36. Jones TH, Morawetz RB, Crowell RM, Marcoux FW, FitzGibbon SJ, DeGirolami U. Thresholds of focal cerebral ischemia in awake monkeys. J Neurosurg. 1981 ; 54 (6). 773-82
37. Kaufmann AM, Firlik AD, Fukui MB, Wechsler LR, Jungries CA, Yonas H. Ischemic core and penumbra in human stroke. Stroke. 1999 ; 30 (1). 93-9
38. Kent DM, Price LL, Ringleb P, Hill MD, Selker HP. Sex-based differences in response to recombinant tissue plasminogen activator in acute ischemic stroke: a pooled analysis of randomized clinical trials. Stroke. 2005 ; 36 (1). 62-5
39. Lay CC, Davis MF, Chen-Bee CH, Frostig RD. Mild sensory stimulation completely protects the adult rodent cortex from ischemic stroke. PLoS One. 2010 ; 5 (6). e11270
40. Lay CC, Davis MF, Chen-Bee CH, Frostig RD Neuroscience 2011. Washington, DC: Society for Neuroscience ; 2011a:
41. Lay CC, Davis MF, Chen-Bee CH, Frostig RD. Mild sensory stimulation reestablishes cortical function during the acute phase of ischemia. J Neurosci. 2011b ; 31 (32). 11495-504
42. Lay CC, Davis MF, Chen-Bee CH, Frostig RD. Mild sensory stimulation protects the aged rodent from cortical ischemic stroke following permanent middle cerebral artery occlusion. J Am Heart Assoc. 2012 ; 1 (4). e001255
43. Liebeskind DS. Collateral circulation. Stroke. 2003 ; 34 (9). 2279-84
44. Lo EH, Dalkara T, Moskowitz MA. Mechanisms, challenges and opportunities in stroke. Nat Rev Neurosci. 2003 ; 4 (5). 399-415
45. Martinez-Vila E, Sieira PI. Current status and perspectives of neuroprotection in ischemic stroke treatment. Cerebrovasc Dis. 2001 ; 11: 60-70
46. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron. 2010 ; 67 (2). 181-98
47. Murphy TH, Corbett D. Plasticity during stroke recovery: from synapse to behaviour. Nat Rev Neurosci. 2009 ; 10 (12). 861-72
48. Nakayama H, Jorgensen HS, Raaschou HO, Olsen TS. The influence of age on stroke outcome. The Copenhagen Stroke Study. Stroke. 1994 ; 25 (4). 808-13
49. Tissue plasminogen activator for acute ischemic stroke. The National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. N Engl J Med. 1995 ; 333 (24). 1581-7
50. NINDS stops trial enrollment in SAMMPRIS trial due to higher risk of stroke and death in stented group. American Academy of Neurology. 2011 ;:
51. Nudo RJ, Eisner-Janowicz I Reprogramming the cerebral cortex: plasticity following central and peripheral lesions. Lomber S Eggermont J, ed. Oxford: Oxford University Press ; 2006: 231-56.
52. Nudo RJ, Plautz EJ, Frost SB. Role of adaptive plasticity in recovery of function after damage to motor cortex. Muscle Nerve. 2001 ; 24 (8). 1000-19
53. Popa-Wagner A, Buga AM, Kokaia Z. Perturbed cellular response to brain injury during aging. Ageing Res Rev. 2011 ; 10 (1). 71-9
54. Popa-Wagner A, Carmichael ST, Kokaia Z, Kessler C, Walker LC. The response of the aged brain to stroke: too much, too soon?. Curr Neurovasc Res. 2007 ; 4 (3). 216-27
55. Roger VL, Go AS, Lloyd-Jones DM, Adams RJ, Berry JD, Brown TM. Heart disease and stroke statistics - 2011 update: a report from the American Heart Association. Circulation. 2011 ; 123 (4). e18-209
56. Saver JL. Time is brain - quantified. Stroke. 2006 ; 37 (1). 263-6
57. Schaffer CB, Friedman B, Nishimura N, Schroeder LF, Tsai PS, Ebner FF. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 2006 ; 4 (2). e22
58. Traversa R, Cicinelli P, Bassi A, Rossini PM, Bernardi G. Mapping of motor cortical reorganization after stroke. A brain stimulation study with focal magnetic pulses. Stroke. 1997 ; 28 (1). 110-7
59. Ts'o DY, Frostig RD, Lieke EE, Grinvald A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science. 1990 ; 249 (4967). 417-20
60. Turner RJ, Jickling GC, Sharp FR. Are underlying assumptions of current animal models of human stroke correct: from STAIRs to high hurdles?. Transl Stroke Res. 2011 ; 2 (2). 138-43
61. Wahlgren NG, Ahmed N. Neuroprotection in cerebral ischaemia: facts and fancies - the need for new approaches. Cerebrovasc Dis. 2004 ; 17: 153-66
62. Wang-Fischer Y Manual of stroke models in rats. Boca Raton, FL: CRC Press ; 2009: 17 239-30 78.
63. Wardlaw JM, Murray V, Berge E, Del Zoppo GJ. Thrombolysis for acute ischaemic stroke. Cochrane Database Syst Rev. 2009 ; (4). CD000213
64. Weber R, Ramos-Cabrer P, Justicia C, Wiedermann D, Strecker C, Sprenger C. Early prediction of functional recovery after experimental stroke: functional magnetic resonance imaging, electrophysiology, and behavioral testing in rats. J Neurosci. 2008 ; 28 (5). 1022-9
65. Wei L, Craven K, Erinjeri J, Liang GE, Bereczki D, Rovainen CM. Local cerebral blood flow during the first hour following acute ligation of multiple arterioles in rat whisker barrel cortex. Neurobiol Dis. 1998 ; 5 (3). 142-50
66. Wintermark M, Reichhart M, Cuisenaire O, Maeder P, Thiran JP, Schnyder P. Comparison of admission perfusion computed tomography and qualitative diffusion- and perfusion-weighted magnetic resonance imaging in acute stroke patients. Stroke. 2002 ; 33 (8). 2025-31
67. Zhang F, Graham SH, Chen J Chen J Xu X-M Xu ZC Zhang JH, ed. New York: Springer ; 2012: 107-14.