Targeted insult to subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke (original) (raw)

References

  1. Hudetz, A.G. Percolation phenomenon: The effect of capillary network rarefaction. Microvasc. Res. 45, 1–10 (1993).
    Article CAS Google Scholar
  2. Moody, D.M., Bell, M.A. & Challa, V.R. Features of the cerebral vascular pattern that predict vulnerability to perfusion or oxygenation deficiency: An anatomic study. AJNR Am. J. Neuroradiol. 11, 431–439 (1990).
    CAS PubMed Google Scholar
  3. Brozici, M., van der Zwain, A. & Hillen, B. Anatomy and functionality of leptomeningeal anastomoses: A review. Stroke 34, 2750–2762 (2003).
    Article Google Scholar
  4. Cox, S.B., Woolsey, T.A. & Rovainen, C.M. Localized dynamic changes in cortical blood flow with whisker stimulation corresponds to matched vascular and neuronal architecture of rat barrels. J. Cereb. Blood Flow Metab. 13, 899–913 (1993).
    Article CAS Google Scholar
  5. Iadecola, C. Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat. Rev. Neurosci. 5, 347–360 (2004).
    Article CAS Google Scholar
  6. Wardlaw, J.M., Sandercock, P.A., Dennis, M.S. & Starr, J. Is breakdown of the blood-brain barrier responsible for lacunar stroke, leukoaraiosis, and dementia? Stroke 34, 806–812 (2003).
    Article CAS Google Scholar
  7. Cullen, K.M., Zoltan, K. & Stone, J . Pericapillary haem-rich deposits: Evidence for microhaemorrhages in aging human cerebral cortex. J. Cereb. Blood Flow Metab. 25, 1656–1667 (2005).
    Article CAS Google Scholar
  8. del Zoppo, G.J. Microvascular changes during cerebral ischemia and reperfusion. Cardiovascular and Brain Metabolism Reviews 6, 47–96 (1994).
    CAS Google Scholar
  9. Farkas, E. & Luiten, P.G.M. Cerebral microvascular pathology in aging and Alzheimer's disease. Prog. Neurobiol. 64, 575–611 (2001).
    Article CAS Google Scholar
  10. Watson, B.D., Dietrich, W.D., Busto, R., Wachtel, M.S. & Ginsberg, M.D. Induction of reproducible brain infarction by photochemically initiated thrombosis. Ann. Neurol. 17, 497–504 (1985).
    Article CAS Google Scholar
  11. Haseldonckx, M., van Bedaf, D., van de Ven, M., van Reempts, J. & Borgers, M. Vasogenic oedema and brain infarction in an experimental penumbra model. Acta Neurochir. (Wien) 76 (Suppl.), 105–109 (2000).
    CAS Google Scholar
  12. Vogel, A. & Venugopalan, V. Mechanisms of pulsed laser ablation of biological tissues. Chem. Rev. 103, 577–644 (2003).
    Article CAS Google Scholar
  13. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161–165 (1997).
    Article CAS Google Scholar
  14. Kleinfeld, D., Mitra, P.P., Helmchen, F. & Denk, W. Fluctuations and stimulus-induced changes in blood flow observed in individual capillaries in layers 2 through 4 of rat neocortex. Proc. Natl. Acad. Sci. USA 95, 15741–15746 (1998).
    Article CAS Google Scholar
  15. Dawson, D.A. & Hallenbeck, J.M. Acute focal ischemia-induced alterations in MAP2 immunostaining: Description of temporal changes and utilization as a marker for volumetric assessment of acute brain injury. J. Cereb. Blood Flow Metab. 16, 170–174 (1996).
    Article CAS Google Scholar
  16. Latov, N. et al. Fibrillary astrocytes proliferate in response to brain injury. Dev. Biol. 72, 381–384 (1979).
    Article CAS Google Scholar
  17. Chapman, J.D., Franko, A.J. & Sharplin, J. A marker for hypoxic cells in tumours with potential clinical applicability. Br. J. Cancer 43, 546–550 (1981).
    Article CAS Google Scholar
  18. Asplund, K. Haemodilution for acute ischaemic stroke (a review). Cochrane Database Syst. Rev. 3, 1–41 (2005).
    Google Scholar
  19. Sakharov, D.V., Barrett-Bergshoeff, M., Hekkenberg, R.T. & Rijken, D.C. Fibrin-specificity of a plasminogen activator affects the efficiency of fibrinolysis and responsiveness to ultrasound: Comparison of nine plasminogen activators in vitro. Thromb. Haemost. 81, 605–612 (1999).
    CAS PubMed Google Scholar
  20. The GUSTO Angiographic Investigators. The effects of tissue plasminogen activator, streptokinase, or both on coronary-artery patency, ventricular function, and survival after acute myocardial infarction. N. Engl. J. Med. 319, 1615–1622 (1993).
  21. Lyden, P.D. Thrombolytic Stroke Therapy, 2nd Edition (Humana Press, New Jersey, 2004).
    Google Scholar
  22. Skalak, R., Chen, P.H. & Chien, S. Effect of hematocrit and rouleaux on apparent viscosity in capillaries. Biorheology 9, 67–83 (1972).
    Article CAS Google Scholar
  23. Goldman, D. & Popel, A.S. A computational study of the effect of capillary network anastomoses and tortuosity on oxygen transport. J. Theor. Biol. 206, 181–194 (2000).
    Article CAS Google Scholar
  24. Schaffer, C.B. et al. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. Public Library of Science, Biology; in the press.
  25. Baron, J.C. Perfusion thresholds in human cerebral ischemia: Historical perspective and therapeutic implications. Cerebrovasc. Dis. 11, 2–8 (2001).
    Article Google Scholar
  26. Hossmann, K.A. Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36, 557–565 (1994).
    Article CAS Google Scholar
  27. Zhao, W., Belayev, L. & Ginsberg, M.D. Transient middle cerebral artery occlusion by intraluminal suture II. Neurological deficits, and pixel-based correlation of histopathology with local blood flow and glucose utilization. J. Cereb. Blood Flow Metab. 17, 1281–1290 (1997).
    Article CAS Google Scholar
  28. O'Brien, J.T. et al. Vascular cognitive impairment. Lancet Neurol. 2, 89–98 (2003).
    Article Google Scholar
  29. Dobrogowska, D.H., Lossinsky, A.S., Tarnawski, M. & Vorbrodt, A.W. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J. Neurocytol. 27, 163–173 (1998).
    Article CAS Google Scholar
  30. Rosenberg, G.A., Mun-Bryce, S., Wesley, M. & Kornfeld, M. Collagenase-induced intracerebral hemorrhage in rats. Stroke 21, 801–807 (1990).
    Article CAS Google Scholar
  31. Dijkhuizen, R.M., Asahi, M., Wu, O., Rosen, B.R. & Lo, E.H. Rapid breakdown of microvascular barriers and subsequent hemorrhagic transformation after delayed recombinant tissue plasminogen activator treatment in a rat embolic stroke model. Stroke 33, 2100–2104 (2002).
    Article CAS Google Scholar
  32. Kaufman, H.H. et al. A rabbit model of intracerebral hematoma. Acta Neuropathol. (Berl.) 65, 318–321 (1985).
    Article CAS Google Scholar
  33. Fazekas, F. et al. Histopathologic analysis of foci of signal loss on gradient-echo T2*-weighted MR images in patients with spontaneous intracerebral hemorrhage: Evidence of microangiopathy-related microbleeds. AJNR Am. J. Neuroradiol. 20, 637–642 (1999).
    CAS PubMed Google Scholar
  34. Lyden, P.D., Jackson-Friedman, C., Shin, C. & Hassid, S. Synergistic combinatorial stroke therapy: A quantal bioassay of a GABA agonist and a glutamate antagonist. Exp. Neurol. 163, 477–489 (2000).
    Article CAS Google Scholar
  35. Longa, E.Z., Weinstein, P.R., Carlson, S. & Cummins, R. Reversible middle cerebral artery occlusion without craniectomy in rats. Stroke 20, 84–91 (1989).
    Article CAS Google Scholar
  36. Wei, L., Rovainen, C.M. & Woolsey, T.A. Ministrokes in rat barrel cortex. Stroke 26, 1459–1462 (1995).
    Article CAS Google Scholar
  37. Yao, H. et al. Photothrombotic middle cerebral artery occlusion and reperfusion laser system in spontaneously hypertensive rats. Stroke 34, 2716–2721 (2003).
    Article Google Scholar
  38. Nakase, H., Kakizaki, T., Miyamoto, K., Hiramatsu, K. & Sakaki, T. Use of local cerebral blood flow monitoring to predict brain damage after disturbance to the venous circulation: Cortical vein occlusion model by photochemical dye. Neurosurgery 37, 280–285 (1995).
    Article CAS Google Scholar
  39. Takeo, S., Miyake, K., Minematsu, R., Tanonaka, K. & Konishi, M. In vitro effect of naftidrofuryl oxalate on cerebral mitochondria impaired by microsphere-induced embolism in rats. J. Pharmacol. Exp. Ther. 248, 1207–1214 (1989).
    CAS PubMed Google Scholar
  40. Kudo, M., Aoyama, A., Ichimori, S. & Fukunaga, N. An animal model of cerebral infarction. Homologous blood clot emboli in rats. Stroke 13, 505–508 (1982).
    Article CAS Google Scholar
  41. Futrell, N. et al. A new model of embolic stroke produced by photochemical injury to the carotid artery in the rat. Ann. Neurol. 23, 251–257 (1988).
    Article CAS Google Scholar
  42. Lo, E.H., Dalkara, T. & Moskowitz, M.A. Mechanisms, challenges and opportunities in stroke. Nat. Rev. Neurosci. 4, 399–415 (2003).
    Article CAS Google Scholar
  43. Kleinfeld, D. & Delaney, K.R. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage sensitive dyes. J. Comp. Neurol. 375, 89–108 (1996).
    Article CAS Google Scholar
  44. Tsai, P.S. et al. Principles, design, and construction of a two photon laser scanning microscope for in vitro and in vivo brain imaging. In In Vivo Optical Imaging of Brain Function (ed. Frostig, R.D. ed.) 113–171 (CRC Press, Boca Raton, 2002).
    Google Scholar
  45. Tsai, P.S. et al. All-optical histology using ultrashort laser pulses. Neuron 39, 27–41 (2003).
    Article CAS Google Scholar
  46. Backus, S. et al. High-efficiency, single-stage 7-kHz high-average-power ultrafast laser system. Opt. Lett. 26, 465–467 (2001).
    Article CAS Google Scholar
  47. Zhang, R.L., Zhang, Z.G. & Chopp, M. Increased therapeutic efficacy with rt-PA and anti-CD18 antibody treatment of stroke in the rat. Neurology 15, 273–279 (1999).
    Article Google Scholar
  48. Korninger, C. & Collen, D. Studies on the specific fibrinolytic effect of human extrinsic (tissue-type) plasminogen activator in human blood and in various animal species in vitro. Thromb. Haemost. 46, 561–565 (1981).
    Article CAS Google Scholar
  49. Scremin, O.U. Cerebral vascular system. In The Rat Nervous System (Paxinos, G. ed.) 3–35 (Academic Press, Inc., San Diego, 1995).
    Google Scholar

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