Rapid and Local Autoregulation of Cerebrovascular Blood Flow: a Deep-brain Imaging Study in the Mouse

Overview

Journal J Physiol

Specialty Physiology

Date 2008 Dec 17

PMID 19074968

Citations 4

Authors

Nahoko Kuga

Tadashi Hirata

Ikuko Sakai

Yoshihisa Tanikawa

Huei Yu Chiou

Takuma Kitanishi

Norio Matsuki

Yuji Ikegaya

Affiliations

Soon will be listed here.

Abstract

The brain obtains energy by keeping the cerebral blood flow constant against unexpected changes in systemic blood pressure. Although this homeostatic mechanism is widely known as cerebrovascular autoregulation, it is not understood how widely and how robustly it works in the brain. Using a needle-like objective lens designed for deep-tissue imaging, we quantified the degree of autoregulation in the mouse hippocampus with single-capillary resolution. On average, hippocampal blood flow exhibited autoregulation over a comparatively broad range of arterial blood pressure and did not significantly respond to pressure changes induced by the pharmacological activation of autonomic nervous system receptors, whereas peripheral tissues showed linear blood flow changes. At the level of individual capillaries, however, about 40% of hippocampal capillaries did not undergo rapid autoregulation. This heterogeneity suggests the presence of a local baroreflex system to implement cerebral autoregulation.

Citing Articles

Beyond neurovascular coupling, role of astrocytes in the regulation of vascular tone.

Filosa J, Morrison H, Iddings J, Du W, Kim K Neuroscience. 2015; 323:96-109.

PMID: 25843438 PMC: 4592693. DOI: 10.1016/j.neuroscience.2015.03.064.

Monitoring of systemic and hepatic hemodynamic parameters in mice.

Xie C, Wei W, Zhang T, Dirsch O, Dahmen U J Vis Exp. 2014; (92):e51955.

PMID: 25350047 PMC: 4692415. DOI: 10.3791/51955.

Large-scale calcium waves traveling through astrocytic networks in vivo.

Kuga N, Sasaki T, Takahara Y, Matsuki N, Ikegaya Y J Neurosci. 2011; 31(7):2607-14.

PMID: 21325528 PMC: 6623677. DOI: 10.1523/JNEUROSCI.5319-10.2011.

Continuous estimates of dynamic cerebral autoregulation during transient hypocapnia and hypercapnia.

Dineen N, Brodie F, Robinson T, Panerai R J Appl Physiol (1985). 2009; 108(3):604-13.

PMID: 20035062 PMC: 2838633. DOI: 10.1152/japplphysiol.01157.2009.

References

Helmchen F, Fee M, Tank D, Denk W . A miniature head-mounted two-photon microscope. high-resolution brain imaging in freely moving animals. Neuron. 2001; 31(6):903-12. DOI: 10.1016/s0896-6273(01)00421-4. View

Villringer A, Them A, Lindauer U, Einhaupl K, Dirnagl U . Capillary perfusion of the rat brain cortex. An in vivo confocal microscopy study. Circ Res. 1994; 75(1):55-62. DOI: 10.1161/01.res.75.1.55. View

Hamel E . Perivascular nerves and the regulation of cerebrovascular tone. J Appl Physiol (1985). 2006; 100(3):1059-64. DOI: 10.1152/japplphysiol.00954.2005. View

Weber B, Keller A, Reichold J, Logothetis N . The microvascular system of the striate and extrastriate visual cortex of the macaque. Cereb Cortex. 2008; 18(10):2318-30. DOI: 10.1093/cercor/bhm259. View

Roman G, Erkinjuntti T, Wallin A, Pantoni L, Chui H . Subcortical ischaemic vascular dementia. Lancet Neurol. 2003; 1(7):426-36. DOI: 10.1016/s1474-4422(02)00190-4. View

Pulsinelli W, BRIERLEY J, Plum F . Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol. 1982; 11(5):491-8. DOI: 10.1002/ana.410110509. View

Knot H, Nelson M . Regulation of arterial diameter and wall [Ca2+] in cerebral arteries of rat by membrane potential and intravascular pressure. J Physiol. 1998; 508 ( Pt 1):199-209. PMC: 2230857. DOI: 10.1111/j.1469-7793.1998.199br.x. View

Dirnagl U, Villringer A, Einhaupl K . In-vivo confocal scanning laser microscopy of the cerebral microcirculation. J Microsc. 1992; 165(Pt 1):147-57. DOI: 10.1111/j.1365-2818.1992.tb04312.x. View

Coyle P . Spatial features of the rat hippocampal vascular system. Exp Neurol. 1978; 58(3):549-61. DOI: 10.1016/0014-4886(78)90108-5. View

10.

Levene M, Dombeck D, Kasischke K, Molloy R, Webb W . In vivo multiphoton microscopy of deep brain tissue. J Neurophysiol. 2003; 91(4):1908-12. DOI: 10.1152/jn.01007.2003. View

11.

Aaslid R, Lindegaard K, Sorteberg W, Nornes H . Cerebral autoregulation dynamics in humans. Stroke. 1989; 20(1):45-52. DOI: 10.1161/01.str.20.1.45. View

12.

Hudetz A . Blood flow in the cerebral capillary network: a review emphasizing observations with intravital microscopy. Microcirculation. 1997; 4(2):233-52. DOI: 10.3109/10739689709146787. View

13.

Lovick T, Brown L, Key B . Neurovascular relationships in hippocampal slices: physiological and anatomical studies of mechanisms underlying flow-metabolism coupling in intraparenchymal microvessels. Neuroscience. 1999; 92(1):47-60. DOI: 10.1016/s0306-4522(98)00737-4. View

14.

Novak V, Novak P, Spies J, Low P . Autoregulation of cerebral blood flow in orthostatic hypotension. Stroke. 1998; 29(1):104-11. DOI: 10.1161/01.str.29.1.104. View

15.

Florence G, Seylaz J . Rapid autoregulation of cerebral blood flow: a laser-Doppler flowmetry study. J Cereb Blood Flow Metab. 1992; 12(4):674-80. DOI: 10.1038/jcbfm.1992.92. View

16.

Grubb B, Gerard G, Roush K, Montford P, Elliott L, Hahn H . Cerebral vasoconstriction during head-upright tilt-induced vasovagal syncope. A paradoxic and unexpected response. Circulation. 1991; 84(3):1157-64. DOI: 10.1161/01.cir.84.3.1157. View

17.

Chaigneau E, Oheim M, Audinat E, Charpak S . Two-photon imaging of capillary blood flow in olfactory bulb glomeruli. Proc Natl Acad Sci U S A. 2003; 100(22):13081-6. PMC: 240748. DOI: 10.1073/pnas.2133652100. View

18.

Iadecola C . Neurovascular regulation in the normal brain and in Alzheimer's disease. Nat Rev Neurosci. 2004; 5(5):347-60. DOI: 10.1038/nrn1387. View

19.

Dodt H, Leischner U, Schierloh A, Jahrling N, Mauch C, Deininger K . Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat Methods. 2007; 4(4):331-6. DOI: 10.1038/nmeth1036. View

20.

Kleinfeld D, Mitra 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 U S A. 1998; 95(26):15741-6. PMC: 28114. DOI: 10.1073/pnas.95.26.15741. View