Compartment-resolved imaging of activity-dependent dynamics of cortical blood volume and oximetry.
Optical imaging, positron emission tomography, and functional magnetic resonance imaging (fMRI) all rely on vascular responses to image neuronal activity. Although these imaging techniques are used successfully for functional brain mapping, the detailed spatiotemporal dynamics of hemodynamic events in the various microvascular compartments have remained unknown. Here we used high-resolution optical imaging in area 18 of anesthetized cats to selectively explore sensory-evoked cerebral blood-volume (CBV) changes in the various cortical microvascular compartments. To avoid the confounding effects of hematocrit and oximetry changes, we developed and used a new fluorescent blood plasma tracer and combined these measurements with optical imaging of intrinsic signals at a near-isosbestic wavelength for hemoglobin (565 nm). The vascular response began at the arteriolar level, rapidly spreading toward capillaries and venules. Larger veins lagged behind. Capillaries exhibited clear blood-volume changes. Arterioles and arteries had the largest response, whereas the venous response was smallest. Information about compartment-specific oxygen tension dynamics was obtained in imaging sessions using 605 nm illumination, a wavelength known to reflect primarily oximetric changes, thus being more directly related to electrical activity than CBV changes. Those images were radically different: the response began at the parenchyma level, followed only later by the other microvascular compartments. These results have implications for the modeling of fMRI responses (e.g., the balloon model). Furthermore, functional maps obtained by imaging the capillary CBV response were similar but not identical to those obtained using the early oximetric signal, suggesting the presence of different regulatory mechanisms underlying these two hemodynamic processes.
Vanzetta
Ivo
I
Department of Neurobiology, Weizmann Institute of Science, Rehovot 76100, Israel. ivo.vanzetta@incm.cnrs-mrs.fr
Hildesheim
Rina
R
Grinvald
Amiram
A
D000818:Animals; D001931:Brain Mapping; D002415:Cats; D002560:Cerebrovascular Circulation / Q000502:physiology*; D003952:Diagnostic Imaging / Q000379:methods; D007091:Image Processing, Computer-Assisted / Q000379:methods; D008279:Magnetic Resonance Imaging; D017711:Nonlinear Dynamics; D010092:Oximetry; D010100:Oxygen / Q000097:blood*; D010775:Photic Stimulation / Q000379:methods; D015203:Reproducibility of Results; D013997:Time Factors; D014793:Visual Cortex / Q000098:blood supply* / Q000502:physiology
D010100:Oxygen
Science. 1996 Apr 26;272(5261):551-4
8614805
J Neurosci. 2003 May 15;23(10):3963-71
12764080
J Neurosci. 1993 Oct;13(10):4157-80
8410182
Hum Brain Mapp. 2001 Dec;14(4):210-7
11668652
Neuron. 2001 Oct 25;32(2):359-74
11684004
J Neurosci Methods. 1991 Feb;36(2-3):127-37
1905769
Neuroimage. 2003 Jul;19(3):884-94
12880817
J Neurosci. 2004 Apr 14;24(15):3850-61
15084666
Science. 1997 Jun 27;276(5321):2034-7
9197264
Proc Natl Acad Sci U S A. 1990 Aug;87(16):6082-6
2117272
Magn Reson Med. 2003 Apr;49(4):655-64
12652536
J Neurosci. 2004 Jan 21;24(3):634-41
14736849
Neuroimage. 2004;23 Suppl 1:S220-33
15501093
Neuroimage. 2000 Apr;11(4):302-12
10725186
Phys Med Biol. 2000 Dec;45(12):3749-64
11131197
J Neurophysiol. 1997 May;77(5):2780-7
9163392
J Physiol. 1949 May;108(3):278-81
18149764
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):13081-6
14569029
Nat Neurosci. 2003 Jan;6(1):5-6
12494240
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10904-9
11526212
Magn Reson Med. 2000 Aug;44(2):231-42
10918322
Neurosci Lett. 2001 Jun 22;306(1-2):106-10
11403969
J Neurosci. 1997 Mar 15;17(6):2112-27
9045738
Neuroimage. 2001 Nov;14(5):977-94
11697930
Science. 1999 Jan 22;283(5401):496-7
9988650
Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15741-6
9861040
Magn Reson Med. 1998 Jun;39(6):855-64
9621908
News Physiol Sci. 1999 Oct;14:177-182
11390847
Science. 1996 Jun 14;272(5268):1665-8
8658144
Proc Natl Acad Sci U S A. 2003 Dec 23;100(26):16000-5
14673091
J Physiol. 1982 Dec;333:269-91
7182467
Microvasc Res. 1998 Jul;56(1):43-53
9683562
Nat Neurosci. 2000 May;3(5):413-4
10769371
Science. 1999 Nov 19;286(5444):1555-8
10567261
Neuroimage. 2002 Sep;17(1):1-18
12482064
Brain Res. 1981 Mar 9;208(1):35-58
7470927
Am J Physiol Heart Circ Physiol. 2000 Apr;278(4):H1294-8
10749727
Neuroimage. 2001 Jun;13(6 Pt 1):975-87
11352604
Cerebrovasc Brain Metab Rev. 1995 Fall;7(3):240-76
8519605
Science. 2003 Feb 14;299(5609):1070-2
12586942
J Physiol. 1890 Jan;11(1-2):85-158.17
16991945
Neuroimage. 1999 Sep;10(3 Pt 1):304-26
10458944
J Neurosci. 1985 Jul;5(7):1886-95
4020423
J Cereb Blood Flow Metab. 1993 Nov;13(6):899-913
8408316
Nature. 1996 Feb 22;379(6567):725-8
8602218
Brain Res. 1983 Dec 19;289(1-2):65-70
6661656
J Physiol. 1973 Jun;231(2):365-83
4352767
Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10625-9
7938003
J Neurosci. 1996 Nov 1;16(21):6945-64
8824332
J Cereb Blood Flow Metab. 2002 Mar;22(3):353-60
11891441
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6417-22
11344262
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4239-44
12655065
Neuroscientist. 2004 Feb;10(1):53-62
14987448
Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14826-31
9405698
Nat Neurosci. 2003 Jan;6(1):43-50
12469126
Trends Neurosci. 2003 Feb;26(2):108-14
12536134
Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12456-61
14530410
Neuroimage. 2001 Jun;13(6 Pt 1):959-67
11352602
Magn Reson Med. 2001 May;45(5):791-800
11323805
Nat Neurosci. 2000 Feb;3(2):105-7
10649563
Cereb Cortex. 2002 Mar;12(3):225-33
11839597
Nature. 1986 Nov 27-Dec 3;324(6095):361-4
3785405
J Neurophysiol. 2002 Sep;88(3):1545-58
12205174
Magn Reson Med. 1997 Jun;37(6):877-84
9178239
Ren Physiol Biochem. 1994 May-Aug;17(3-4):168-71
7518950
Neuroimage. 1998 May;7(4 Pt 1):326-36
9626673
J Neurosci. 1991 May;11(5):1458-69
1851222
Nature. 1991 Oct 3;353(6343):429-31
1896085
Neuron. 2004 Jun 10;42(5):843-54
15182722
Nat Neurosci. 2000 Feb;3(2):164-9
10649572
Neuroimage. 2001 Jun;13(6 Pt 1):988-1001
11352605
J Cereb Blood Flow Metab. 1997 Jan;17(1):64-72
8978388