Time-varying spreading depression waves in rat cortex revealed by optical intrinsic signal imaging

This study aimed to investigate the variation of propagation patterns of successive spreading depression (SD) waves induced by K+ in rat cortex. SD was elicited by 1 M KCl solution in the frontal cortex of 18 Sprague-Dawley rats under alpha-chloralose/urethane anesthesia. We applied optical intrinsic signal imaging (OISI) at an isosbestic point of hemoglobin (550 nm) to examine regional cerebral blood volume (CBV) changes in the parieto-occipital cortex. In 6 of the 18 rats, OISI was performed in conjunction with DC potential recording of the cortex. CBV changes appeared as repetitive propagation of wave-like hyperemia at a speed of 3.7+/-0.4 mm/min, which was characterized by a significant negative peak (-14.3+/-3.2%) in the reflectance signal. Among the observed 186 SDs, the first wave always propagated through the entire imaged cortex in every rat, whereas following waves were likely to bypass the medial area of the imaged cortex (partially propagated waves, n=65, 35%). Correspondingly, DC potential shifts showed non-uniform in the medial area, and they seemed closely related to the changes in reflectance. For partially propagated SD waves, the mean time interval to the previous SD wave (217.0+/-24.3 s) was significantly shorter than for fully propagated SD waves (251.2+/-29.0 s). The results suggest that the propagation patterns of a series of SD waves are time-varying in different regions of rat cortex, and the variation is related to the interval between SD waves.

[1]  Andrew K. Dunn,et al.  Intrinsic brain activity triggers trigeminal meningeal afferents in a migraine model , 2002, Nature Medicine.

[2]  Li Peng.  In vivo Optical Imaging of Intrinsic Signal During Cortical Spreading Depression in Rats , 2003 .

[3]  A. A. P. Leo,et al.  PIAL CIRCULATION AND SPREADING DEPRESSION OF ACTIVITY IN THE CEREBRAL CORTEX , 1944 .

[4]  Arthur W. Toga,et al.  Characterization of optical intrinsic signals and blood volume during cortical spreading depression , 2000, Neuroreport.

[5]  H C Kwan,et al.  Characterization of cortical spreading depression by imaging of intrinsic optical signals. , 1996, Neuroreport.

[6]  M. Lauritzen,et al.  Pathophysiology of the migraine aura. The spreading depression theory. , 1994, Brain : a journal of neurology.

[7]  Kai Simons,et al.  Fusion of Constitutive Membrane Traffic with the Cell Surface Observed by Evanescent Wave Microscopy , 2000, The Journal of cell biology.

[8]  Jens Haueisen,et al.  Inhomogeneous propagation of cortical spreading depression—detection by electro- and magnetoencephalography in rats , 2004, Brain Research.

[9]  A. Grinvald,et al.  Vascular imprints of neuronal activity: relationships between the dynamics of cortical blood flow, oxygenation, and volume changes following sensory stimulation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Joel H Greenberg,et al.  Cortical Spreading Depression Causes a Long-Lasting Decrease in Cerebral Blood Flow and Induces Tolerance to Permanent Focal Ischemia in Rat Brain , 2003, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[11]  Nader Pouratian,et al.  Multiwavelength optical intrinsic signal imaging of cortical spreading depression. , 2002, Journal of neurophysiology.

[12]  Thomas T. Liu,et al.  Analysis and Design of Perfusion-Based Event-Related fMRI Experiments , 2002, NeuroImage.

[13]  Stefan Müller,et al.  Dispersion relation of spreading depression waves in the chicken retina , 1997 .

[14]  S. Schuchmann,et al.  Intrinsic Optical Imaging Reveals Regionally Different Manifestation of Spreading Depression in Hippocampal and Entorhinal Structures in Vitro , 2002, Experimental Neurology.

[15]  E. Fifková.  SPREADING EEG DEPRESSION IN THE NEO-, PALEO- AND ARCHICORTICAL STRUCTURES OF THE BRAIN OF THE RAT. , 1964, Physiologia bohemoslovenica.

[16]  G. Somjen.  Mechanisms of spreading depression and hypoxic spreading depression-like depolarization. , 2001, Physiological reviews.

[17]  G. Paxinos.  The Rat nervous system , 1985 .

[18]  Charles Nicholson,et al.  Perspectives on spreading depression , 2000, Brain Research Reviews.

[19]  A. A. Leão,et al.  SPREADING DEPRESSION OF ACTIVITY IN THE CEREBRAL CORTEX , 1944 .

[20]  Yutaka Tomita,et al.  Repetitive concentric wave-ring spread of oligemia/hyperemia in the sensorimotor cortex accompanying K+-induced spreading depression in rats and cats , 2002, Neuroscience Letters.

[21]  J. L. Stringer,et al.  Astrocytes contribute to regulation of extracellular calcium and potassium in the rat cerebral cortex during spreading depression , 2004, Brain Research.

[22]  Shaoqun Zeng,et al.  Spatiotemporal characteristics of cerebral blood volume changes in rat somatosensory cortex evoked by sciatic nerve stimulation and obtained by optical imaging. , 2003, Journal of biomedical optics.