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The Journal of Neuroscience, November 3, 2004, 24(44):9897-9902; doi:10.1523/JNEUROSCI.2705-04.2004
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Spiral Waves in Disinhibited Mammalian Neocortex
Xiaoying Huang,1
William C. Troy,2
Qian Yang,1
Hongtao Ma,1
Carlo R. Laing,3
Steven J. Schiff,4 and
Jian-Young Wu1
1Department of Physiology and Biophysics, Georgetown University Medical Center, Washington, DC 20057, 2Department of Mathematics, University of Pittsburgh, Pittsburgh, Pennsylvania 15260, 3Department of Mathematics, Massey University, 102-904 Auckland, New Zealand, and 4Department of Psychology and Program in Neuroscience, Krasnow Institute, George Mason University, Fairfax, Virginia 22030
Spiral waves are a basic feature of excitable systems. Although such waves have been observed in a variety of biological systems, they have not been observed in the mammalian cortex during neuronal activity. Here, we report stable rotating spiral waves in rat neocortical slices visualized by voltage-sensitive dye imaging. Tissue from the occipital cortex (visual) was sectioned parallel to cortical lamina to preserve horizontal connections in layers III-V (500-µm-thick, 4 x 6 mm2). In such tangential slices, excitation waves propagated in two dimensions during cholinergic oscillations. Spiral waves occurred spontaneously and alternated with plane, ring, and irregular waves. The rotation rate of the spirals was 10 turns per second, and the rotation was linked to the oscillations in a one-cycle- one-rotation manner. A small (<128 µm) phase singularity occurred at the center of the spirals, about which were observed oscillations of widely distributed phases. The phase singularity drifted slowly across the tissue ( 1 mm/10 turns). We introduced a computational model of a cortical layer that predicted and replicated many of the features of our experimental findings. We speculate that rotating spiral waves may provide a spatial framework to organize cortical oscillations.
Key words: voltage-sensitive dye; tangential slice; optical imaging; oscillation; partial differential equations; spiral waves
Received July 7, 2004;
revised September 8, 2004;
accepted September 10, 2004.
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