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The Journal of Neuroscience, April 18, 2007, 27(16):4452-4459; doi:10.1523/JNEUROSCI.0134-07.2007

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Behavioral/Systems/Cognitive
Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal

Anna Devor,^1,4 Peifang Tian,¹ Nozomi Nishimura,² Ivan C. Teng,¹ Elizabeth M. C. Hillman,⁴ S. N. Narayanan,⁴ Istvan Ulbert,^4,5 David A. Boas,⁴ David Kleinfeld,² and Anders M. Dale^1,3

Departments of ¹Neurosciences, ²Physics, and ³Radiology, University of California, San Diego, California 92093, ⁴Massachusetts General Hospital, Harvard Medical School, Charlestown, Massachusetts 02129, and ⁵Institute for Psychology of the Hungarian Academy of Sciences, Budapest 1068, Hungary

Correspondence should be addressed to either of the following: Anna Devor or David Kleinfeld, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093; Email: adevor{at}ucsd.edu or Email: dk{at}physics.ucsd.edu

Synaptic transmission initiates a cascade of signal transduction events that couple neuronal activity to local changes in blood flow and oxygenation. Although a number of vasoactive molecules and specific cell types have been implicated, the transformation of stimulus-induced activation of neuronal circuits to hemodynamic changes is still unclear. We use somatosensory stimulation and a suite of in vivo imaging tools to study neurovascular coupling in rat primary somatosensory cortex. Our stimulus evoked a central region of net neuronal depolarization surrounded by net hyperpolarization. Hemodynamic measurements revealed that predominant depolarization corresponded to an increase in oxygenation, whereas predominant hyperpolarization corresponded to a decrease in oxygenation. On the microscopic level of single surface arterioles, the response was composed of a combination of dilatory and constrictive phases. Critically, the relative strength of vasoconstriction covaried with the relative strength of oxygenation decrease and neuronal hyperpolarization. These results suggest that a neuronal inhibition and concurrent arteriolar vasoconstriction correspond to a decrease in blood oxygenation, which would be consistent with a negative blood oxygenation level-dependent functional magnetic resonance imaging signal.

Key words: hemodynamic; somatosensory; two-photon; voltage-sensitive dyes; intrinsic imaging; electrode array

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Received Jan. 11, 2007; revised March 17, 2007; accepted March 19, 2007.

Correspondence should be addressed to either of the following: Anna Devor or David Kleinfeld, University of California at San Diego, 9500 Gilman Drive, La Jolla, CA 92093; Email: adevor{at}ucsd.edu or Email: dk{at}physics.ucsd.edu

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