Investigating neural-hemodynamic coupling and the hemodynamic response function in the awake rat

NeuroImage

Volumn 32, Issue 1, 2006, Pages 33-48

  Martin, Chris ^a   Martindale, John ^a   Berwick, Jason ^a   Mayhew, John ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANESTHETIC AGENT; OXYGEN;

ANIMAL; ARTICLE; BLOOD; BRAIN; BRAIN CIRCULATION; DRUG EFFECT; HEMODYNAMICS; NERVE CELL; PHYSIOLOGY; RAT; SOMATOSENSORY CORTEX; VASCULARIZATION; WAKEFULNESS;

ANESTHETICS; ANIMALS; BRAIN; CEREBROVASCULAR CIRCULATION; HEMODYNAMIC PROCESSES; NEURONS; OXYGEN; RATS; SOMATOSENSORY CORTEX; WAKEFULNESS;

EID: 33748637368     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2006.02.021     Document Type: Article

References (86)

1. Ahissar, E., Sosnik, R., Haidarliu, S., 2000. Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406 (6793), 302-306.
2. Ances, B.M., Zarahn, E., Greenberg, J.H., Detre, J.A., 2000. Coupling of neural activation to blood flow in the somatosensory cortex of rats is time-intensity separable, but not linear. J. Cereb. Blood Flow Metab. 20 (6), 921-930.
3. Armstrong-James, M., Fox, K., Das-Gupta, A., 1992. Flow of excitation within rat barrel cortex on striking a single vibrissa. J. Neurophysiol. 68 (4), 1345-1358.
4. Austin, V.C., Blamire, A.M., Allers, K.A., Sharp, T., Styles, P., Matthews, P.M., Sibson, N.R., 2005. Confounding effects of anesthesia on functional activation in rodent brain: a study of halothane and alphachloralose anesthesia. NeuroImage 24 (1), 92-100.
5. Bandettini, P.A., Cox, R.W., 2000. Event-related fMRI contrast when using constant interstimulus interval: theory and experiment. Magn. Reson. Med. 43 (4), 540-548.
6. Berwick, J., Martin, C., Martindale, J., Jones, M., Johnston, D., Zheng, Y., Redgrave, P., Mayhew, J., 2002. Hemodynamic response in the unanesthetized rat: intrinsic optical imaging and spectroscopy of the barrel cortex. J. Cereb. Blood Flow Metab. 22 (6), 670-679.
7. Bonvento, G., Charbonne, R., Correze, J.L., Borredon, J., Seylaz, J., Lacombe, P., 1994. Is alpha-chloralose plus halothane induction a suitable anesthetic regimen for cerebrovascular research Brain Res. 665 (2), 213-221.
8. Buxton, R.B., 2001. The elusive initial dip. NeuroImage 13 (6 Pt. 1), 953-958.
9. Buxton, R.B., Frank, L.R., 1997. A model for the coupling between cerebral blood flow and oxygen metabolism during neural stimulation. J. Cereb. Blood Flow Metab. 17 (1), 64-72.
10. Caesar, K., Gold, L., Lauritzen, M., 2003. Context sensitivity of activitydependent increases in cerebral blood flow. Proc. Natl. Acad. Sci. U. S. A. 100 (7), 4239-4244.
11. Castro-Alamancos, M.A., 2002. Different temporal processing of sensory inputs in the rat thalamus during quiescent and information processing states in vivo. J. Physiol. 539 (Pt. 2), 567-578.
12. Castro-Alamancos, M.A., Oldford, E., 2002. Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J. Physiol. 541 (Pt. 1), 319-331.
13. Chapin, J.K., Waterhouse, B.D., Woodward, D.J., 1981. Differences in cutaneous sensory response properties of single somatosensory cortical neurons in awake and halothane anesthetized rats. Brain Res. Bull. 6 (1), 63-70.
14. Cohen, L.B., 1973. Changes in neuron structure during action potential propagation and synaptic transmission. Physiol. Rev. 53 (2), 373-418.
15. Cox, S.B., Woolsey, T.A., Rovainen, C.M., 1993. 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 (6), 899-913.
16. Devilbiss, D.M., Waterhouse, B.D., 2002. Determination and quantification of pharmacological, physiological, or behavioral manipulations on ensembles of simultaneously recorded neurons in functionally related neural circuits. J. Neurosci. Methods 121 (2), 181-198.
17. Devor, A., Dunn, A.K., Andermann, M.L., Ulbert, I., Boas, D.A., Dale, A.M., 2003. Coupling of total hemoglobin concentration, oxygenation, and neural activity in rat somatosensory cortex. Neuron 39 (2), 353-359.
18. Devor, A., Ulbert, I., Dunn, A.K., Narayanan, S.N., Jones, S.R., Andermann, M.L., Boas, D.A., Dale, A.M., 2005. Coupling of the cortical hemodynamic response to cortical and thalamic neuronal activity. Proc. Natl. Acad. Sci. U. S. A. 102 (10), 3822-3827.
19. Dunn, A.K., Devor, A., Bolay, H., Andermann, M.L., Moskowitz, M.A., Dale, A.M., Boas, D.A., 2003. Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation. Opt. Lett. 28 (1), 28-30.
20. Ernst, T., Hennig, J., 1994. Observation of a fast response in functional MR. Magn. Reson. Med. 32 (1), 146-149.
21. Fanselow, E.E., Nicolelis, M.A., 1999. Behavioral modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19 (17), 7603-7616.
22. Feng, C.M., Liu, H.L., Fox, P.T., Gao, J.H., 2003. Dynamic changes in the cerebral metabolic rate of O2 and oxygen extraction ratio in eventrelated functional MRI. NeuroImage 18 (2), 257-262.
23. Gerrits, R.J., Raczynski, C., Greene, A.S., Stein, E.A., 2000. Regional cerebral blood flow responses to variable frequency whisker stimulation: an autoradiographic analysis. Brain Res. 864 (2), 205-212.
24. Gerrits, R.J., Stein, E.A., Greene, A.S., 1998. Blood flow increases linearly in rat somatosensory cortex with increased whisker movement frequency. Brain Res. 783 (1), 151-157.
25. Grubb, R.L. Jr., Raichle, M.E., Eichling, J.O., Ter-Pogossian, M.M., 1974. The effects of changes in PaCO2 on cerebral blood volume, blood flow, and vascular mean transit time. Stroke 5 (5), 630-639.
26. Hewson-Stoate, N., Jones, M., Martindale, J., Berwick, J., Mayhew, J., 2005. Further nonlinearities in neurovascular coupling in rodent barrel cortex. NeuroImage 24 (2), 565-574.
27. Hoge, R.D., Atkinson, J., Gill, B., Crelier, G.R., Marrett, S., Pike, G.B., 1999. Investigation of BOLD signal dependence on cerebral blood flow and oxygen consumption: the deoxyhemoglobin dilution model. Magn. Reson. Med. 42 (5), 849-863.
28. Hoge, R.D., Atkinson, J., Gill, B., Crelier, G.R., Marrett, S., Pike, G.B., 1999. Linear coupling between cerebral blood flow and oxygen consumption in activated human cortex. Proc. Natl. Acad. Sci. U. S. A. 96 (16), 9403-9408.
29. Hoge, R.D., Franceschini, M.A., Covolan, R.J., Huppert, T., Mandeville, J.B., Boas, D.A., 2005. Simultaneous recording of task-induced changes in blood oxygenation, volume, and flow using diffuse optical imaging and arterial spin-labeling MRI. NeuroImage 25 (3), 701-707.
30. Hu, X., Le, T.H., Ugurbil, K., 1997. Evaluation of the early response in fMRI in individual subjects using short stimulus duration. Magn. Reson. Med. 37 (6), 877-884.
31. Hyder, F., Rothman, D.L., Shulman, R.G., 2002. Total neuroenergetics support localized brain activity: implications for the interpretation of fMRI. Proc. Natl. Acad. Sci. U. S. A. 99 (16), 10771-10776.
32. Hyder, F., Shulman, R.G., Rothman, D.L., 1998. A model for the regulation of cerebral oxygen delivery. J. Appl. Physiol. 85 (2), 554-564.
33. Ito, H., Kanno, I., Ibaraki, M., Hatazawa, J., Miura, S., 2003. Changes in human cerebral blood flow and cerebral blood volume during hypercapnia and hypocapnia measured by positron emission tomography. J. Cereb. Blood Flow Metab. 23 (6), 665-670.
34. Janz, C., Schmitt, C., Speck, O., Hennig, J., 2000. Comparison of the hemodynamic response to different visual stimuli in single-event and block stimulation fMRI experiments. J. Magn. Reson. Imaging 12 (5), 708-714.
35. Jones, E.G., Diamond, I.T., 1995. Cerebral Cortex. The Barrel Cortex of Rodents. Plenum Press, New York.
36. Jones, M., Berwick, J., Johnston, D., Mayhew, J., 2001. Concurrent optical imaging spectroscopy and laser-Doppler flowmetry: the relationship between blood flow, oxygenation, and volume in rodent barrel cortex. NeuroImage 13 (6 Pt. 1), 1002-1015.
37. Jones, M., Berwick, J., Mayhew, J., 2002. Changes in blood flow, oxygenation, and volume following extended stimulation of rodent barrel cortex. NeuroImage 15 (3), 474-487.
38. Jones, M., Hewson-Stoate, N., Martindale, J., Redgrave, P., Mayhew, J., 2004. Nonlinear coupling of neural activity and CBF in rodent barrel cortex. NeuroImage 22 (2), 956-965.
39. Kaisti, K.K., Langsjo, J.W., Aalto, S., Oikonen, V., Sipila, H., Teras, M., Hinkka, S., Metsahonkala, L., Scheinin, H., 2003. Effects of sevoflurane, propofol, and adjunct nitrous oxide on regional cerebral blood flow, oxygen consumption, and blood volume in humans. Anesthesiology 99 (3), 603-613.
40. Kennerley, A.J., Berwick, J., Martindale, J., Johnston, D., Papadakis, N., Mayhew, J.E., 2005. Concurrent fMRI and optical measures for the investigation of the hemodynamic response function. Magn. Reson. Med. 54 (2), 354-365.
41. Kim, S.G., Rostrup, E., Larsson, H.B., Ogawa, S., Paulson, O.B., 1999. Determination of relative CMRO2 from CBF and BOLD changes: significant increase of oxygen consumption rate during visual stimulation. Magn. Reson. Med. 41 (6), 1152-1161.
42. Kleinfeld, D., Mitra, P.P., Helmchen, F., Denk, W., 1998. 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. 95 (26), 15741-15746.
43. Kong, Y., Zheng, Y., Johnston, D., Martindale, J., Jones, M., Billings, S., Mayhew, J., 2004. A model of the dynamic relationship between blood flow and volume changes during brain activation. J. Cereb. Blood Flow Metab. 24 (12), 1382-1392.
44. Lahti, K.M., Ferris, C.F., Li, F., Sotak, C.H., King, J.A., 1998. Imaging brain activity in conscious animals using functional MRI. J. Neurosci. Methods 82 (1), 75-83.
45. Lahti, K.M., Ferris, C.F., Li, F., Sotak, C.H., King, J.A., 1999. Comparison of evoked cortical activity in conscious and propofol-anesthetized rats using functional MRI. Magn. Reson. Med. 41 (2), 412-416.
46. Lindauer, U., Villringer, A., Dirnagl, U., 1993. Characterization of CBF response to somatosensory stimulation: model and influence of anesthetics. Am. J. Physiol. 264 (4 Pt. 2), H1223-H1228.
47. Linde, R., Schmalbruch, I.K., Paulson, O.B., Madsen, P.L., 1999. The Kety-Schmidt technique for repeated measurements of global cerebral blood flow and metabolism in the conscious rat. Acta Physiol. Scand. 165 (4), 395-401.
48. Logothetis, N.K., 2003. The underpinnings of the BOLD functional magnetic resonance imaging signal. J. Neurosci. 23 (10), 3963-3971.
49. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T., Oeltermann, A., 2001. Neurophysiological investigation of the basis of the fMRI signal. Nature 412 (6843), 150-157.
50. Malonek, D., Grinvald, A., 1996. Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: implications for functional brain mapping. Science 272 (5261), 551-554.
51. Malonek, D., Dirnagl, U., Lindauer, U., Yamada, K., Kanno, I., Grinvald, A., 1997. Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. Proc. Natl. Acad. U.S.A. 94 (26), 14826-14831.
52. Mandeville, J.B., Marota, J.J., Ayata, C., Zaharchuk, G., Moskowitz, M.A., Rosen, B.R., Weisskoff, R.M., 1999. Evidence of a cerebrovascular postarteriole windkessel with delayed compliance. J. Cereb. Blood Flow Metab. 19 (6), 679-689.
53. Martin, C., Berwick, J., Johnston, D., Zheng, Y., Martindale, J., Port, M., Redgrave, P., Mayhew, J., 2002. Optical imaging spectroscopy in the unanaesthetised rat. J. Neurosci. Methods 120 (1), 25-34.
54. Martindale, J., Mayhew, J., Berwick, J., Jones, M., Martin, C., Johnston, D., Redgrave, P., Zheng, Y., 2003. The hemodynamic impulse response to a single neural event. J. Cereb Blood Flow Metab. 23 (5), 546-555.
55. Mathiesen, C., Caesar, K., Akgoren, N., Lauritzen, M., 1998. Modification of activity-dependent increases of cerebral blood flow by excitatory synaptic activity and spikes in rat cerebellar cortex. J. Physiol. 512 (Pt. 2), 555-566.
56. Matsuura, T., Fujita, H., Seki, C., Kashikura, K., Yamada, K., Kanno, I., 1999. CBF change evoked by somatosensory activation measured by laser-Doppler flowmetry: independent evaluation of RBC velocity and RBC concentration. Jpn. J. Physiol. 49 (3), 289-296.
57. Mayhew, J., Zhao, L., Hou, Y., Berwick, J., Askew, S., Zheng, Y., Coffey, P., 1998. Spectroscopic investigation of reflectance changes in the barrel cortex following whisker stimulation. Adv. Exp. Med. Biol. 454, 139-148.
58. Menon, R.S., Ogawa, S., Hu, X., Strupp, J.P., Anderson, P., Ugurbil, K., 1995. BOLD based functional MRI at 4 Tesla includes a capillary bed contribution: echo-planar imaging correlates with previous optical imaging using intrinsic signals. Magn. Reson. Med. 33 (3), 453-459.
59. Mitzdorf, U., 1987. Properties of the evoked potential generators: current source-density analysis of visually evoked potentials in the cat cortex. Int. J. Neurosci. 33 (1-2), 33-59.
60. Molgedey, L., Schuster, H.G., 1994. Separation of a mixture of independent signals using time delayed correlations. Phys. Rev. Lett. 72, 3634-3637.
61. Moskalenko, Y.E., Dowling, J.L., Liu, D., Rovainen, C.M., Semernia, V.N., Woolsey, T.A., 1996. LCBF changes in rat somatosensory cortex during whisker stimulation monitored by dynamic H2 clearance. Int. J. Psychophysiol. 21 (1), 45-59.
62. Nakao, Y., Itoh, Y., Kuang, T.Y., Cook, M., Jehle, J., Sokoloff, L., 2001. Effects of anesthesia on functional activation of cerebral blood flow and metabolism. Proc. Natl. Acad. Sci. U. S. A. 98 (13), 7593-7598.
63. Nemoto, M., Sheth, S., Guiou, M., Pouratian, N., Chen, J.W., Toga, A.W., 2004. Functional signal- and paradigm-dependent linear relationships between synaptic activity and hemodynamic responses in rat somatosensory cortex. J. Neurosci. 24 (15), 3850-3861.
64. Ngai, A.C., Jolley, M.A., D'Ambrosio, R., Meno, J.R., Winn, H.R., 1999. Frequency-dependent changes in cerebral blood flow and evoked potentials during somatosensory stimulation in the rat. Brain Res. 837 (1-2), 221-228.
65. Nielsen, A.N., Lauritzen, M., 2001. Coupling and uncoupling of activitydependent increases of neuronal activity and blood flow in rat somatosensory cortex. J. Physiol. 533 (Pt. 3), 773-785.
66. Osborne, P.G., 1997. Hippocampal and striatal blood flow during behavior in rats: chronic laser Doppler flowmetry study. Physiol. Behav. 61 (4), 485-492.
67. Oz, G., Berkich, D.A., Henry, P.G., Xu, Y., LaNoue, K., Hutson, S.M., Gruetter, R., 2004. Neuroglial metabolism in the awake rat brain: CO2 fixation increases with brain activity. J. Neurosci. 24 (50), 11273-11279.
68. Peeters, R.R., Tindemans, I., De Schutter, E., Van der Linden, A., 2001. Comparing BOLD fMRI signal changes in the awake and anesthetized rat during electrical forepaw stimulation. Magn. Reson. Imaging 19 (6), 821-826.
69. Poggio, G.F., Mountcastle, V.B., 1963. The functional properties of ventrobasal thalamic neurons studied in unanesthetized monkeys. J. Neurophysiol. 26, 775-806.
70. Rostrup, E., Knudsen, G.M., Law, I., Holm, S., Larsson, H.B., Paulson, O.B., 2005. The relationship between cerebral blood flow and volume in humans. NeuroImage 24 (1), 1 -11.
71. Sachdev, R.N., Champney, G.C., Lee, H., Price, R.R., Pickens, D.R. III, Morgan, V.L., Stefansic, J.D., Melzer, P., Ebner, F.F., 2003. Experimental model for functional magnetic resonance imaging of somatic sensory cortex in the unanesthetized rat. NeuroImage 19 (3), 742-750.
72. Sheth, S., Nemoto, M., Guiou, M., Walker, M., Pouratian, N., Toga, A.W., 2003. Evaluation of coupling between optical intrinsic signals and neuronal activity in rat somatosensory cortex. NeuroImage 19 (3), 884-894.
73. Sheth, S.A., Nemoto, M., Guiou, M., Walker, M., Pouratian, N., Toga, A.W., 2004. Linear and nonlinear relationships between neuronal activity, oxygen metabolism, and hemodynamic responses. Neuron 42 (2), 347-355.
74. Shtoyerman, E., Arieli, A., Slovin, H., Vanzetta, I., Grinvald, A., 2000. Long-term optical imaging and spectroscopy reveal mechanisms underlying the intrinsic signal and stability of cortical maps in V1 of behaving monkeys. J. Neurosci. 20 (21), 8111 -8121.
75. Sicard, K., Shen, Q., Brevard, M.E., Sullivan, R., Ferris, C.F., King, J.A., Duong, T.Q., 2003. Regional cerebral blood flow and BOLD responses in conscious and anesthetized rats under basal and hypercapnic conditions: implications for functional MRI studies. J. Cereb. Blood Flow Metab. 23 (4), 472-481.
76. Smith, A.J., Blumenfeld, H., Behar, K.L., Rothman, D.L., Shulman, R.G., Hyder, F., 2002. Cerebral energetics and spiking frequency: the neurophysiological basis of fMRI. Proc. Natl. Acad. Sci. U. S. A. 99 (16), 10765-10770.
77. Thompson, J.K., Peterson, M.R., Freeman, R.D., 2003. Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299 (5609), 1070-1072.
78. Ureshi, M., Matsuura, T., Kanno, I., 2004. Stimulus frequency dependence of the linear relationship between local cerebral blood flow and field potential evoked by activation of rat somatosensory cortex. Neurosci. Res. 48 (2), 147-153.
79. Vanzetta, I., Grinvald, A., 2001. Evidence and lack of evidence for the initial dip in the anesthetized rat: implications for human functional brain imaging. NeuroImage 13 (6 Pt. 1), 959-967.
80. Vogel, J., Kuschinsky, W., 1996. Decreased heterogeneity of capillary plasma flow in the rat whisker-barrel cortex during functional hyperemia. J. Cereb. Blood Flow Metab. 16 (6), 1300-1306.
81. Woolsey, T.A., Rovainen, C.M., Cox, S.B., Henegar, M.H., Liang, G.E., Liu, D., Moskalenko, Y.E., Sui, J., Wei, L., 1996. Neuronal units linked to microvascular modules in cerebral cortex: response elements for imaging the brain. Cereb. Cortex 6 (5), 647-660.
82. Wu, G., Luo, F., Li, Z., Zhao, X., Li, S.J., 2002. Transient relationships among BOLD, CBV, and CBF changes in rat brain as detected by functional MRI. Magn. Reson. Med. 48 (6), 987-993.
83. Wyrwicz, A.M., Chen, N., Li, L., Weiss, C., Disterhoft, J.F., 2000. fMRI of visual system activation in the conscious rabbit. Magn. Reson. Med. 44 (3), 474-478.
84. Yacoub, E., Shmuel, A., Pfeuffer, J., Van De Moortele, P.F., Adriany, G., Ugurbil, K., Hu, X., 2001. Investigation of the initial dip in fMRI at 7 Tesla. NMR Biomed. 14 (7-8), 408-412.
85. Zheng, Y., Johnston, D., Berwick, J., Mayhew, J., 2001. Signal source separation in the analysis of neural activity in brain. NeuroImage 13 (3), 447-458.
86. Zheng, Y., Martindale, J., Johnston, D., Jones, M., Berwick, J., Mayhew, J., 2002. A model of the hemodynamic response and oxygen delivery to brain. NeuroImage 16 (3 Pt. 1), 617-637.