Pial arteriole dilation during somatosensory stimulation is not mediated by an increase in CSF metabolites

Abstract

Ngai, Al C., and H. Richard Winn. Pial arteriole dilation during somatosensory stimulation is not mediated by an increase in CSF metabolites. Am J Physiol Heart Circ Physiol 282: H902-H907, 2002; 10.1152/ajpheart.00128.2001.-Pial arterioles supplying the hindlimb somatosensory cortex dilate in response to contralateral sciatic nerve stimulation. The mechanism of this pial vasodilation is not well understood. One possibility is that vasoactive metabolites released during brain activation may diffuse to subarachnoid cerebrospinal fluid (CSF) to dilate pial vessels. To test this hypothesis, we implanted closed cranial windows in rats and measured pial arteriolar dilation to sciatic nerve stimulation during constant rate superfusion of the pial surface with artificial CSF. We reason that flushing the pial surface with CSF should quickly dissipate vasoactive substances and prevent these substances from dilating pial arterioles. CSF flow (1 and 1.5 ml/min) significantly reduced pial arteriole dilation induced by 5% CO 2 inhalation, but the same flow rates did not affect dilator responses to sciatic nerve stimulation. We conclude that brain-to-CSF diffusion of vasoactive metabolites does not play a significant role in the dilation of pial arterioles during somatosensory activity. cerebral blood flow; coupling; hypercapnia CEREBRAL ACTIVATION by sensory stimulation is accompanied by adjustments of vascular resistance and blood flow in the activated region. For example, we (13) have shown that pial arterioles supplying the hindlimb somatosensory cortex dilate in response to contralateral sciatic nerve stimulation. The mechanism of this pial vasodilation remains unclear. One possibility is that neuronal activity evoked by sensory stimulation causes the release of metabolites, which may diffuse to subarachnoid cerebrospinal fluid (CSF) to dilate pial arterioles. Putative vasoactive metabolites released during cortical synaptic activity include adenosine, H ϩ , K ϩ , and nitric oxide (1, 6). A variation of this diffusion mechanism is an arteriolar-venular countercurrent scheme (5) involving 1) the release of a vasodilator substance in the brain parenchyma and 2) the transport of the vasoactive substance by the draining venules to the pial surface.The present study tested this diffusion hypothesis. We reasoned that flushing the pial surface with CSF should quickly dissipate vasoactive substances and prevent these substances from dilating pial arterioles. We also studied the effect of CSF superfusion on dilation induced by hypercapnia. Moving CSF has previously been shown to attenuate hypercapnic vasodilation of pial arterioles, presumably by washing away perivascular CO 2 released locally from the vascular compartment (9). METHODSExperimental protocols in the present study were approved by the Animal Care Committee of the University of Washington. Adult male Sprague-Dawley rats weighing between 350 and 400 g were initially anesthetized with 2% halothane. The right femoral artery was exposed and cannulated for arterial blood ...

Inflow effects on hemodynamic responses characterized by event‐related using gradient‐echo EPI sequences

“…In the macrovasculature, the time-of-flight ͑TOF͒ effect is sensitive to blood flow velocity change and may enhance stimuli-induced BOLD contrast. The TOF contrast was observed previously in pial arterial vessels 34,35 as well as in cerebral cortical veins ͑23% flow velocity increase͒. 36 A recent study demonstrated that the variation of the HR ͑e.g., time-to-peak and FWHM͒ depended on vessel diameters, orientations, and the flow velocity contained within a voxel.…”

Coupling Mechanism and Significance of the BOLD Signal: A Status Report

“…Specific branches of pial arteries also dilate rapidly, extending up to >1 mm away from the center of the responding region (Li et al 2003, Ngai & Winn 2002) with recent evidence supporting high-speed retrograde propagation of vasodilation (Chen et al 2011, Iadecola et al 1997, Chen et al 2014). …”

Mechanical restriction of intracortical vessel dilation by brain tissue sculpts the hemodynamic response

“…This would require that vasoactive transmitters diffuse tens to hundreds of microns to the pial vessels. Ngai and Winn (2002) directly tested the hypothesis that surface vessels respond to spillover of vasodilators by flushing the pial vessels with ACSF during sensory stimulation. They found that flushing the pial surface with ACSF had no effect on sensory evoked dilation of pial arterioles, but did reduce CO 2 evoked dilation, supporting the idea that CO 2 dilates vessels via a different pathway than neural activity.…”