The smallest stroke: Occlusion of one penetrating vessel leads to infarction and a cognitive deficit

Nature Neuroscience

Volumn 16, Issue 1, 2013, Pages 55-63

  Shih, Andy Y ^a,c   Blinder, Pablo ^a,d   Tsai, Philbert S ^a   Friedman, Beth ^a   Stanley, Geoffrey ^a   Lyden, Patrick D ^b   Kleinfeld, David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CEDARS SINAI MEDICAL CENTER   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^d TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

DIZOCILPINE; MEMANTINE;

ALZHEIMER DISEASE; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL OCCLUSION; BLOOD VOLUME; BRAIN BLOOD VESSEL; BRAIN CORTEX; BRAIN INFARCTION; BRAIN INJURY; CEREBROVASCULAR ACCIDENT; COGNITIVE DEFECT; MALE; MULTIINFARCT DEMENTIA; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; BRAIN INFARCTION; BRAIN MAPPING; CALCIUM; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; DIZOCILPINE MALEATE; GLIAL FIBRILLARY ACIDIC PROTEIN; HUMANS; IMAGING, THREE-DIMENSIONAL; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; MEMANTINE; MICROSCOPY, CONFOCAL; MICROVESSELS; MODELS, BIOLOGICAL; NEURAL PATHWAYS; NEUROPROTECTIVE AGENTS; PHOSPHOPYRUVATE HYDRATASE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, LONG-EVANS; RATS, SPRAGUE-DAWLEY; SOMATOSENSORY CORTEX; VIBRISSAE;

EID: 84871712919     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3278     Document Type: Article

References (60)

1. Gorelick, P.B. et al. Vascular contributions to cognitive impairment and dementia: a statement for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 42, 2672-2713 (2011).
2. Brundel, M., de Bresser, J., van Dillen, J.J., Kappelle, L.J. & Biessels, G.J. Cerebral microinfarcts: a systematic review of neuropathological studies. J. Cereb. Blood Flow Metab. 32, 425-436 (2012).
3. Smith, E.E., Schneider, J.A., Wardlaw, J.M. & Greenberg, S.M. Cerebral microinfarcts: the invisible lesions. Lancet Neurol. 11, 272-282 (2012).
4. Vinters, H.V. et al. Neuropathologic substrates of ischemic vascular dementia. J. Neuropathol. Exp. Neurol. 59, 931-945 (2000).
5. Kövari, E. et al. Cortical microinfarcts and demyelination affect cognition in cases at high risk for dementia. Neurology 68, 927-931 (2007).
6. Arvanitakis, Z., Leurgans, S.E., Barnes, L.L., Bennett, D.A. & Schneider, J.A. Microinfarct pathology, dementia and cognitive systems. Stroke 42, 722-727 (2011).
7. Jouvent, E. et al. Intracortical infarcts in small vessel disease: a combined 7-T postmortem MRI and neuropathological case study in cerebral autosomal-dominant arteriopathy with subcortical infarcts and leukoencephalopthy. Stroke 42, 27-30 (2011).
8. Blinder, P., Shih, A.Y., Rafie, C.A. & Kleinfeld, D. Topological basis for the robust distribution of blood to rodent neocortex. Proc. Natl. Acad. Sci. USA 107, 12670-12675 (2010).
9. Lauwers, F., Cassot, F., Lauwers-Cances, V., Puwanarajah, P. & Duvernoy, H. Morphometry of the human cerebral cortex microcirculation: general characteristics and space-related profiles. Neuroimage 39, 936-948 (2008).
10. Bär, T. The vascular system of the cerebral cortex. Adv. Anat. Embryol. Cell Biol. 59, 1-62 (1980).
11. Nishimura, N., Schaffer, C.B., Friedman, B., Lyden, P.D. & Kleinfeld, D. Penetrating arterioles are a bottleneck in the perfusion of neocortex. Proc. Natl. Acad. Sci. USA 104, 365-370 (2007).
12. Nguyen, J., Nishimura, N., Fetcho, R.N., Iadecola, C. & Schaffer, C.B. Occlusion of cortical ascending venules causes blood flow decreases, reversals in flow direction, and vessel dilation in upstream capillaries. J. Cereb. Blood Flow Metab. 31, 2243-2254 (2011).
13. Drew, P.J. et al. Chronic optical access through a polished and reinforced thinned skull. Nat. Methods 7, 981-984 (2010).
14. Sofroniew, M.V. & Vinters, H.V. Astrocytes: biology and pathology. Acta Neuropathol. 119, 7-35 (2010).
15. Tsai, P.S. et al. Correlations of neuronal and microvascular densities in murine cortex revealed by direct counting and colocalization of cell nuclei and microvessels. J. Neurosci. 29, 14553-14570 (2009).
16. Weber, B., Keller, A.L., Reichold, J. & Logothetis, N.K. The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb. Cortex 18, 2318-2330 (2008).
17. Svoboda, K., Denk, W., Kleinfeld, D. & Tank, D.W. In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385, 161-165 (1997).
18. 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).
19. Shih, A.Y. et al. Active dilation of penetrating arterioles restores red blood cell flux to penumbral neocortex after focal stroke. J. Cereb. Blood Flow Metab. 29, 738-751 (2009).
20. Shih, A.Y. et al. Two-photon microscopy as a tool to study blood flow and neurovascular coupling in the rodent brain. J. Cereb. Blood Flow Metab. 32, 1277-1309 (2012).
21. Schaffer, C.B. et al. Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion. PLoS Biol. 4, e22 (2006).
22. Nishimura, N. et al. Targeted insult to individual subsurface cortical blood vessels using ultrashort laser pulses: three models of stroke. Nat. Methods 3, 99-108 (2006).
23. Stosiek, C., Garaschuk, O., Holthoff, K. & Konnerth, A. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl. Acad. Sci. USA 100, 7319-7324 (2003).
24. Chen, B. et al. Severe blood brain barrier disruption and surrounding tissue injury. Stroke 40, 666-674 (2009).
25. Calabrese, V., Mancuso, C., Calvani, M., Rizzarelli, E. & Butterfield, D.A. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat. Rev. Neurosci. 8, 766-775 (2007).
26. Friedman, B. et al. Acute vascular disruption and Aquaporin 4 loss after stroke. Stroke 40, 2182-2190 (2009).
27. Unal Cevik, I. & Dalkara, T. Intravenously administered propidium iodide labels necrotic cells in the intact mouse brain after injury. Cell Death Differ. 10, 928-929 (2003).
28. Soontornniyomkij, V. et al. Cerebral microinfarcts associated with severe cerebral beta-amyloid angiopathy. Brain Pathol. 20, 459-467 (2010).
29. Siesjô, B.K. & Bengtsson, F. Calcium fluxes, calcium antagonists and calcium-related pathology in brain ischemia, hypoglycemia, and spreading depression: a unifying hypothesis. J. Cereb. Blood Flow Metab. 9, 127-140 (1989).
30. Murphy, T.H., Li, P., Betts, K. & Liu, R. Two-photon imaging of stroke onset in vivo reveals that NMDA receptor-independent ischemic depolarization is the major cause of rapid reversible damage to dendrites and spines. J. Neurosci. 28, 1756-1772 (2008).
31. Orgogozo, J.M., Rigaud, A.S., Stoffler, A., Mobius, H.J. & Forette, F. Efficacy and safety of Memantine in patients with mild to moderate vascular dementia. Stroke 33, 1834-1839 (2002).
32. Olivares, D. et al. N-Methyl D-Aspartate (NMDA) receptor antagonists and memantine treatment for Alzheimer's disease, vascular dementia and Parkinson's disease. Curr. Alzheimer Res. 9, 746-758 (2012).
33. Woolsey, T.A. & Van Der Loos, H. The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex. Brain Res. 17, 205-242 (1970).
34. Kleinfeld, D. & Deschênes, M. Neuronal basis for object location in the vibrissa scanning sensorimotor system. Neuron 72, 455-468 (2011).
35. Hutson, K.A. & Masterton, R.B. The sensory contribution of a single vibrissa's cortical barrel. J. Neurophysiol. 56, 1196-1223 (1986).
36. Masino, S.A., Kwon, M.C., Dory, Y. & Frostig., R.D. Characterization of functional organization within rat barrel cortex using intrinsic signal optical imaging through a thinned skull. Proc. Natl. Acad. Sci. USA 90, 9998-10002 (1993).
37. Armstrong-James, M., Fox, K. & Das-Gupta, A. Flow of excitability within barrel cortex on striking a single vibrissa. J. Neurophysiol. 68, 1345-1358 (1992).
38. Lashley, K.S. Mass action in cerebral function. Science 73, 245-254 (1931).
39. Reisberg, B. et al. Memantine in moderate-to-severe Alzheimer's disease. N. Engl. J. Med. 348, 1333-1341 (2003).
40. Wilcock, G.K. Memantine for the treatment of dementia. Lancet Neurol. 2, 503-505 (2003).
41. Woolsey, T.A. et al. Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb. Cortex 6, 647-660 (1996).
42. Cassot, F. et al. Branching patterns for arterioles and venules of the human cerebral cortex. Brain Res. 1313, 62-78 (2010).
43. Villringer, A., Mehraein, S. & Einhäupl, K.M. Pathophysiological aspects of cerebral sinus venous thrombosis (SVT). J. Neuroradiol. 21, 72-80 (1994).
44. Brown, W.R. & Thore, C.R. Cerebral microvascular pathology in aging and neurodegeneration. Neuropathol. Appl. Neurobiol. 37, 56-74 (2011).
45. Zhang, S. & Murphy, T.H. Imaging the impact of cortical microcirculation on synaptic structure and sensory-evoked hemodynamic responses in vivo. PLoS Biol. 5, e119 (2007).
46. Troncoso, E. et al. Recovery of evoked potentials, metabolic activity and behavior in a mouse model of somatosensory cortex lesion: role of the neural cell adhesion molecule (NCAM). Cereb. Cortex 14, 332-341 (2004).
47. Carmichael, S.T. Plasticity of cortical projections after stroke. Neuroscienist 9, 64-75 (2003).
48. Mohajerani, M.H., Aminoltejari, K. & Murphy, T.H. Targeted mini-strokes produce changes in interhemispheric sensory signal processing that are indicative of disinhibition within minutes. Proc. Natl. Acad. Sci. USA 108, E183-E191 (2011).
49. Rosidi, N.L. et al. Cortical microhemorrhages cause local inflammation but do not trigger widespread dendrite degeneration. PLoS ONE 6, e26612 (2011).
50. Nishimura, N., Rosidi, N.L., Iadecola, C. & Schaffer, C.B. Limitations of collateral flow after occlusion of a single cortical penetrating arteriole. J. Cereb. Blood Flow Metab. 30, 1914-1927 (2010).
51. Frostig, R.D., Lieke, E.E., Ts'o, D.Y. & 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. USA 87, 6082-6086 (1990).
52. 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).
53. Tsai, P.S. & Kleinfeld, D. In vivo two-photon laser scanning microscopy with concurrent plasma-mediated ablation: principles and hardware realization. in Methods for In Vivo Optical Imaging 2nd edn. (ed. Frostig, R.D.) 59-115 (CRC Press, 2009).
54. Valmianski, I. et al. Automatic identification of fluorescently labeled brain cells for rapid functional imaging. J. Neurophysiol. 104, 1803-1811 (2010).
55. Driscoll, J.D., Shih, A.Y., Drew, P.J., Cauwenberghs, G. & Kleinfeld, D. Two-photon imaging of blood flow in cortex. in Imaging in Neuroscience: A Laboratory Manual (eds. Helmchen, F., Konnerth, A. & Yuste, R.) 927-938 (Cold Spring Harbor Laboratory Press, New York, 2011).
56. Shih, A.Y. et al. Optically induced occlusion of single blood vessels in neocortex. in Imaging in Neuroscience: A Laboratory Manual (eds. Helmchen, F., Konnerth, A. & Yuste, R.) 939-948 (Cold Spring Harbor Laboratory Press, New York, 2011).
57. Nguyen, Q.-T., Dolnick, E.M., Driscoll, J. & Kleinfeld, D. MPScope 2.0: A computer system for two-photon laser scanning microscopy with concurrent plasma-mediated ablation and electrophysiology. in Methods for In Vivo Optical Imaging 2nd edn. (ed. Frostig, R.D.) 117-142 (CRC Press, 2009).
58. Nimmerjahn, A., Kirchhoff, F., Kerr, J.N. & Helmchen, F. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo. Nat. Methods 1, 31-37 (2004).
59. Mehta, S.B., Whitmer, D., Figueroa, R., Williams, B.A. & Kleinfeld, D. Active spatial perception in the vibrissa scanning sensorimotor system. PLoS Biol. 5, 309-322 (2007).
60. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Academic Press, San Diego, 1986).