Contribution of hemodynamics and light scattering to the changes in optical intrinsic signal during cortical spreading depression in rats

Abstract

Optical intrinsic signals (OIS) imaging has been shown a powerful method for characterizing the spatial and temporal pattern of the propagation of cortical spreading depression (CSD) with high resolution. However, the possible physiological mechanisms underlying these OIS during CSD still remain incompletely understood. In this study, spectroscopic recording of the changes in OIS during pinprick induced CSD were performed at the exposed cortex of -chloralose/urethane anesthetized Sprague-Dawley rats (male, n=12) using a fiber optic reflectance spectrometer (PC-1000, Ocean Optics Inc.) to estimate the contribution of hemodynamics and light scattering to the changes in OIS. The fiber probe (source-detector fiber separation: 0.2 mm) was placed at cortical parenchyma site avoiding large blood vessels. For each animal, five CSDs were elicited with an interval of half an hour. On each CSD induction, the spectra data was collected over a 400 seconds period at the rate of 2 Hz. The changes in the concentration of HbO2 and Hb, and changes in light scattering was estimated by fitting the experimental reflectance spectra data to a modified Beer-Lambert equation using a linear least squares fitting procedure, for a spectral range of 460630 nm. The fit was good with a residual error less than 5% in most experiments. In this experiment, four-phasic changes in OIS were observed at 460 nm 570 nm, but triphasic changes were observed at longer wavelength. The fitting results showed that the CSD induced an initial increase in concentration of HbO2 (amplitude: 9.03.7%), which was 26.218.6 s earlier than the onset of increase of Hb concentration. The increase in concentration of Hb reached its maximum value 47.25.9 s earlier than that of HbO2. Whereas the concentration of HbO2 showed a four-phasic change, the light scattering showed a triphasic change and the concentration of Hb only showed a biphasic change. The timing relationship between OIS and concentration of HbO2 and Hb indicated that the initial phase of the decreased IOS at 550 nm was only caused by the concentration increase of oxygenated hemoglobin at cortical parenchyma sites. But during the second phase of the increased optical reflectance at 550 nm, more complicated physiological mechanisms may be involved, not only the changes in concentration of HbO2, Hb and Hbt, but also the changes in light scattering contributed significantly to the increase of optical reflectance. When the concentration of HbO2 shows a small decrease (7.84.5%), the concentration of Hb increased 24.510.8%, simultaneously with a significant increase of light scattering. Interestingly, in our previous studies, a slight constriction of the pial arteries was observed during this phase of OIS. The constriction of the pial artery and the increase of concentration of total hemoglobin at cortical parenchyma site suggest that the regulations of the pial artery and capillary during this phase may be controlled by different mechanisms. During the followed third phase of light decrease at 550 nm, an increase of blood volume (concentration of total hemoglobin), an increase of oxygenation and decrease of scattering all contributed to the change of intrinsic optical signal.