Interactions between electrical activity and cortical microcirculation revealed by imaging spectroscopy: Implications for functional brain mapping

Science

Volumn 272, Issue 5261, 1996, Pages 551-554

  Malonek, Dov ^a   Grinvald, Amiram ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN HYPOXIA; BRAIN MAPPING; BRAIN MICROCIRCULATION; ELECTROENCEPHALOGRAM; IMAGING; NONHUMAN; PRIORITY JOURNAL; SENSORY STIMULATION; SPECTROSCOPY;

EID: 0029997609     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.272.5261.551     Document Type: Article

References (51)

1. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
2. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
3. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
4. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
5. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
6. C. Roy and C. Sherrington, J. Physiol. 11, 85 (1890), J. Olesen, Brain 94, 635 (1971), J. Risberg and D. Ingvar, Brain Res. 96, 737 (1973); M. Kato, H. Ueno, P. Black, Exp. Neurol 42, 65 (1974); J. Greenberg, P. Hand, A. Sylvestro, M. Reivich, Acta Neurol. Scand 60, 12 (1979), C. Iadecola, Trends Neurosci. 16, 206 (1993)
7. P. Fox and M. Raichle, Ann. Neurol. 17, 303 (1985); L. Sokoloff et al., J. Neurochem. 28, 897 (1994); N. A. Lassen and D. H. Ingvar, Experientia 17, 42 (1961)
8. P. Fox and M. Raichle, Ann. Neurol. 17, 303 (1985); L. Sokoloff et al., J. Neurochem. 28, 897 (1994); N. A. Lassen and D. H. Ingvar, Experientia 17, 42 (1961)
9. P. Fox and M. Raichle, Ann. Neurol. 17, 303 (1985); L. Sokoloff et al., J. Neurochem. 28, 897 (1994); N. A. Lassen and D. H. Ingvar, Experientia 17, 42 (1961)
10. M. Raichle, Sci. Am. 270, 58 (April 1994); P. T. Fox et al., Nature 323, 806 (1986), P. Fox and M. Raichle, Proc. Natl. Acad Sci. U.S.A. 83, 1140 (1986), P. T. Fox, M. E. Raichle, M. A. Mintun, C. Dence, Science 241, 462 (1988).
11. M. Raichle, Sci. Am. 270, 58 (April 1994); P. T. Fox et al., Nature 323, 806 (1986), P. Fox and M. Raichle, Proc. Natl. Acad Sci. U.S.A. 83, 1140 (1986), P. T. Fox, M. E. Raichle, M. A. Mintun, C. Dence, Science 241, 462 (1988).
12. M. Raichle, Sci. Am. 270, 58 (April 1994); P. T. Fox et al., Nature 323, 806 (1986), P. Fox and M. Raichle, Proc. Natl. Acad Sci. U.S.A. 83, 1140 (1986), P. T. Fox, M. E. Raichle, M. A. Mintun, C. Dence, Science 241, 462 (1988).
13. M. Raichle, Sci. Am. 270, 58 (April 1994); P. T. Fox et al., Nature 323, 806 (1986), P. Fox and M. Raichle, Proc. Natl. Acad Sci. U.S.A. 83, 1140 (1986), P. T. Fox, M. E. Raichle, M. A. Mintun, C. Dence, Science 241, 462 (1988).
14. S. Ogawa, T. Lee, A. Kay, Proc. Natl. Acad. Sci. U S.A 87, 9868 (1990), J. W. Belliveau et al., Science 254, 716 (1991); K. Kwong et al., Proc Natl. Acad. Sci. U.S.A. 89, 5675 (1992), S. Ogawa et al., ibid , p. 5951; R. Turner et al., Magn. Reson. Med. 29, 277 (1993).
15. S. Ogawa, T. Lee, A. Kay, Proc. Natl. Acad. Sci. U S.A 87, 9868 (1990), J. W. Belliveau et al., Science 254, 716 (1991); K. Kwong et al., Proc Natl. Acad. Sci. U.S.A. 89, 5675 (1992), S. Ogawa et al., ibid , p. 5951; R. Turner et al., Magn. Reson. Med. 29, 277 (1993).
16. S. Ogawa, T. Lee, A. Kay, Proc. Natl. Acad. Sci. U S.A 87, 9868 (1990), J. W. Belliveau et al., Science 254, 716 (1991); K. Kwong et al., Proc Natl. Acad. Sci. U.S.A. 89, 5675 (1992), S. Ogawa et al., ibid , p. 5951; R. Turner et al., Magn. Reson. Med. 29, 277 (1993).
17. S. Ogawa, T. Lee, A. Kay, Proc. Natl. Acad. Sci. U S.A 87, 9868 (1990), J. W. Belliveau et al., Science 254, 716 (1991); K. Kwong et al., Proc Natl. Acad. Sci. U.S.A. 89, 5675 (1992), S. Ogawa et al., ibid , p. 5951; R. Turner et al., Magn. Reson. Med. 29, 277 (1993).
18. S. Ogawa, T. Lee, A. Kay, Proc. Natl. Acad. Sci. U S.A 87, 9868 (1990), J. W. Belliveau et al., Science 254, 716 (1991); K. Kwong et al., Proc Natl. Acad. Sci. U.S.A. 89, 5675 (1992), S. Ogawa et al., ibid , p. 5951; R. Turner et al., Magn. Reson. Med. 29, 277 (1993).
19. A. Grinvald, E Lieke, R Frostig, C Gilbert, T. Wiesel, Nature 324, 361 (1986).
20. D. Y. Ts'o, R. D Frostig, E. E. Lieke, A. Grinvald, Science 249, 417 (1990); G Blasdel, J. Neurosci 12, 3139 (1992); M. Weliky, K. Kandler, D. Fitzpatrick, L C Katz, Neuron 15, 541 (1995); I. Godecke and T. Bonhoeffer, Nature 379, 251 (1996).
21. D. Y. Ts'o, R. D Frostig, E. E. Lieke, A. Grinvald, Science 249, 417 (1990); G Blasdel, J. Neurosci 12, 3139 (1992); M. Weliky, K. Kandler, D. Fitzpatrick, L C Katz, Neuron 15, 541 (1995); I. Godecke and T. Bonhoeffer, Nature 379, 251 (1996).
22. D. Y. Ts'o, R. D Frostig, E. E. Lieke, A. Grinvald, Science 249, 417 (1990); G Blasdel, J. Neurosci 12, 3139 (1992); M. Weliky, K. Kandler, D. Fitzpatrick, L C Katz, Neuron 15, 541 (1995); I. Godecke and T. Bonhoeffer, Nature 379, 251 (1996).
23. D. Y. Ts'o, R. D Frostig, E. E. Lieke, A. Grinvald, Science 249, 417 (1990); G Blasdel, J. Neurosci 12, 3139 (1992); M. Weliky, K. Kandler, D. Fitzpatrick, L C Katz, Neuron 15, 541 (1995); I. Godecke and T. Bonhoeffer, Nature 379, 251 (1996).
24. T. Bonhoeffer and A Grinvald, Nature 353, 429 (1991); J. Neurosci. 13, 4157 (1993).
25. T. Bonhoeffer and A Grinvald, Nature 353, 429 (1991); J. Neurosci. 13, 4157 (1993).
26. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
27. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
28. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
29. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
30. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
31. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
32. B. Chance, P. Cohen, F Jobsis, B. Schoener, Science 137, 499 (1962); L B. Cohen, R D. Keynes, B. Hille, Nature 218, 438 (1968), I Tasaki, A. Watanabe, R. Sandlin, L. Carnay, Proc. Natl. Acad. Sci. U.S.A. 61, 883 (1968), L Cohen, Physiol. Rev. 53, 373 (1973); F Jobsis, J. Keizer, J LaManna, M. Rosental, J. Appl. Physiol. 43, 858 (1977); A. Grinvald, A. Manker, M. Segal, J. Physiol. 333, 269 (1982); B. M. Salzberg et al , Nature 306, 36 (1983).
33. R Frostig, E Lieke, D. Ts'o, A. Grinvald, Proc Natl. Acad Sci. U.S.A 87, 6082 (1990); B MacVicar and D. Hochman, J Neurosci. 11, 1458 (1991)
34. R Frostig, E Lieke, D. Ts'o, A. Grinvald, Proc Natl. Acad Sci. U.S.A 87, 6082 (1990); B MacVicar and D. Hochman, J Neurosci. 11, 1458 (1991)
35. U. Heinrich, J Hoffmann, D. Lubbers, Pflugers Arch. 409, 152 (1987), M. Watanabe, N. Harada, H. Kosaka, T. Shiga, J. Cereb. Blood Flow Metab 14, 75 (1994)
36. U. Heinrich, J Hoffmann, D. Lubbers, Pflugers Arch. 409, 152 (1987), M. Watanabe, N. Harada, H. Kosaka, T. Shiga, J. Cereb. Blood Flow Metab 14, 75 (1994)
37. Five cats were anesthetized with continuous infusion of sodium pentothal after an initial induction using ketamine HCl and atropine sulphate. All surgical and experimental procedures were in accordance with NIH guidelines. A craniotomy was performed, overlying area 18 of the visual cortex. A stainless steel chamber was mounted over the craniotomy. Each stimulus was presented 24 to 128 times, in randomized order. The intrinsic optical signals were imaged by a slow-scan CCD (charge-coupled device) camera (6) or enhanced video system (Imager 2001, Optical Imaging, Germantown) attached to a dual macroscope (22).
38. D. Hubel and T. Wiesel, J. Physiol. 160, 106 (1962).
39. To calculate the mapping spectra, we first computed the global signal spectrum for every cortical location in images obtained during vertical-grating and horizontal-grating stimulation. Each spatiospectral mapping image was then calculated as a difference between the above images Each average mapping spectrum (Fig. 2H) was calculated as the difference between the average spectra from regions that were maximally activated by the vertical grating and the average spectra from regions maximally activated by the horizontal grating.
40. 2 Modeling the contribution from cytochromes proved that at the wavelength range we used, their contribution to the observed spectral changes was minimal.
41. Each mapping component was calculated as a difference between the corresponding global components obtained during vertical and horizontal grating stimulation. We then calculated the difference in the average intensity in regions that were maximally selective for either stimulus.
42. A distinction between the various components of light scattering has not been made here The LS signal is useful for functional optical imaging, whenever large vascular noise is associated with an experiment. High-quality functional maps were obtained at a wavelength longer than 660 nm, at which the contribution of light scattering to the mapping components was larger than 70%.
43. Both f-MRI and PET studies were performed on awake human subjects, whereas the present experiments were performed on anesthetized cats. However, we observed a similar "initial dip" in experiments performed on awake monkeys.
44. I Silver, in Cerebral Vascular Smooth Muscle and its Control, K Elliott and M O'Connor, Eds. (Elsevier, New York, 1978), pp 49-61.
45. R. Menon, X. Hu, P. Andersen, K. Ugurbil, S Ogawa, Proc. Soc. Magn. Reson 1, 68 (1994); J. Henning, T. Ernst, O. Speck, G.Deuscht, E Feifel, Magn Reson. Med. 31, 85 (1994).
46. R. Menon, X. Hu, P. Andersen, K. Ugurbil, S Ogawa, Proc. Soc. Magn. Reson 1, 68 (1994); J. Henning, T. Ernst, O. Speck, G.Deuscht, E Feifel, Magn Reson. Med. 31, 85 (1994).
47. W. Kuschinsky and O. Paulson, Cerebrovasc Brain Metab. Rev. 4, 261 (1992), U. Dirnagl (personal communication) visualized it directly using confocal microscopy.
48. W. Kuschinsky and O. Paulson, Cerebrovasc Brain Metab. Rev. 4, 261 (1992), U. Dirnagl (personal communication) visualized it directly using confocal microscopy.
49. R. Turner and A Grinvald, Proc. Soc. Magn Reson. 1, 430 (1994).
50. H. Ratzlaff and A Grinvald, J. Neurosci. Methods 36, 127 (1991).
51. We thank U Dirnagl, A Villringer, I. Steinberg, A Artsen, and R. Malach for their useful comments. We also thank I. Silver, P. Jezzard, B. Chance, and R Turner for their helpful contribution. Special thanks to A. Ariel, D. Glaser, D. Shoham, A Shmuel, and I Vanzetta for their help during experiments and to N Dekel, D. Ettner, C. Wijnbergen, and S. Leytus for their technical help.