Lack of Sympathetic and Cholinergic Influences on Cerebral Vasodilation Caused by Sciatic Nerve Stimulation in the Rat

Ibayashi, Setsuro; Ngai, Al C.; Howard, Matthew A.; Meno, Joseph R.; Mayberg, Marc R.; Winn, H. Richard

doi:10.1038/jcbfm.1991.120

Cited by 18 publications

(10 citation statements)

References 30 publications

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“…The presence of such vasodilator neurons has, however, never been convincingly demonstrated. Moreover, alterations of sympathetic and parasympathetic cholinergic mechanisms by superior cervical ganglionectomy, atropine application, and lesioning of cholinergic input did not affect the pial dilator response to sciatic nerve stimulation (7). Pial arterioles may also dilate by a shear stress-dependent mechanism (4,14).…”

Section: Discussionmentioning

confidence: 99%

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

Ngai

Winn

2002

American Journal of Physiology-Heart and Circulatory Physiology

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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 ...

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Section: Discussionmentioning

confidence: 99%

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

Ngai

Winn

2002

American Journal of Physiology-Heart and Circulatory Physiology

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“…Zhang et al, 1995). Although its lesion does not alter the changes in CBF induced by neural activity (Ibayashi et al, 1991), this pathway may contribute to maintain resting CBF and modulate the increases in CBF produced by somatosensory activation (Iadecola et al, 1983; Lecrux and Hamel, 2016; Lecrux et al, 2017). On the other hand, cortical norepinephrine levels, which depend in large part on the noradrenergic innervation from the locus coeruleus, have been shown to increase the vasoconstrictor tone in cerebral cortex and help focus oxygen delivery to the activated areas (Bekar et al, 2012).…”

Section: Neurovascular Couplingmentioning

confidence: 99%

The Neurovascular Unit Coming of Age: A Journey through Neurovascular Coupling in Health and Disease

Iadecola

2017

Neuron

1,646

1,649

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The concept of neurovascular unit (NVU), formalized at the 2001 Stroke Progress Review Group meeting of the National Institute of Neurological Disorders and Stroke, emphasizes the intimate relationship between the brain and its vessels. Since then, the NVU has attracted the interest of the neuroscience community resulting in considerable advances in the field. Here the current state-of-knowledge of the NVU will be assessed, focusing on one of its most vital roles: the coupling between neural activity and blood flow. The evidence supports a conceptual shift in the mechanisms of neurovascular coupling, from a unidimensional process involving neuronal-astrocytic signaling to local blood vessels, to a multidimensional one in which mediators released from multiple cells engage distinct signaling pathways and effector systems across the entire cerebrovascular network in a highly orchestrated manner. The recently appreciated NVU dysfunction in neurodegenerative diseases, although still poorly understood, supports emerging concepts that maintaining neurovascular health promotes brain health.

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“…Additionally, we have recently shown that there is no local increase in interstitial adenosine in the hindlimb sensory-motor cortex and that the adenosine antagonist 8-sulfophenyltheophylline fails to block the increase in flow associated with sciatic nerve stimulation (34). Furthermore, the local increase in cortical blood flow in response to peripheral nerve stimulation is not mediated through adrenergic or cholinergic receptors (35).…”

Section: Discussionmentioning

confidence: 99%

Competitive inhibition of nitric oxide synthase prevents the cortical hyperemia associated with peripheral nerve stimulation.

Northington

Matherne

Berne

1992

Proc. Natl. Acad. Sci. U.S.A.

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With combined microdialysis and hydrogen clearance techniques for simultaneous local delivery of drugs and blood-flow measurement in the rat hindlimb sensorymotor cortex, we examined the role of nitric oxide in cerebral blood-flow regulation during sciatic nerve stimulation. Infusion of 1 mM nitric oxide synthase antagonist, N'1-nitro-L-arginine methyl ester (L-NAME), blocked the cortical blood-flow response to sciatic nerve stimulation (152 ± 43 ml mint.100 g't of tissue in controls and 73 + 11 ml-min-l 100 go I in the presence of L-NAME; P < 0.05). Addition of 10 mM L-arginine to the dialysate containing L-NAME partially restored the hyperemic response to nerve stimulation (125 ml mind.100 go ). L-NAME also produced a decrease in baseline cerebral blood flow when compared with the control (66 ± 14 ml mind 100 g-vs. 93 + 25 ml-min-t.100 g-l). We conclude that nitric oxide from activated neurons participates in the local regulation of cortical blood flow in response to sciatic nerve stimulation and also in the maintenance of basal cortical blood flow.The mechanisms regulating cerebral blood flow in response to peripheral nerve stimulation have not been clearly defined. The regional nature of the response strongly suggests that a locally produced vasoactive mediator is involved. Nitric oxide is produced by neurons and astroglia in response to stimulation by excitatory amino acids (1-6) and by nonadrenergic, noncholinergic vasodilator nerves (7,8). It also participates in cell-signaling events in the brain (9-11). Computer modeling suggests that nitric oxide is a mediator in the local regulation of cerebral blood flow during cortical activation (12), but this has not been proven.The present study was designed to determine if nitric oxide participates in the regulation of cerebral blood flow in response to peripheral nerve stimulation. To accomplish this, the combined microdialysis and hydrogen-clearance techniques were used for local drug administration and simultaneous cerebral blood-flow measurement, respectively, in the hindlimb sensory-motor cortex in response to sciatic nerve stimulation. Experiments were performed in the presence and absence of the competitive nitric oxide synthase inhibitor N'-nitro-t,-arginine methyl ester (L-NAME) and in the presence of both L-NAME and the nitric oxide precursor, L-arginine. The effect of L-NAME on baseline cortical blood flow was also determined. MATERIAL AND METHODSPreparation. Adult male Wistar rats (300-450 g) were used. The animal's head was secured in a stereotaxic frame for bilateral placement of the microdialysis cannulas in the hindlimb sensory-motor cortex. The coordinates for this area (1.5-4 mm lateral and 0.3-3 mm posterior to the bregma) were obtained from a stereotaxic atlas (13). A 2 x 2 mm area of the skull was removed with a variable-speed drill over the posterior parietal cortex but away from the hindlimb area to allow for horizontal introduction of the cannulas into the superficial cortex with a micromanipulator. A thin layer of bone was left i...

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Lack of Sympathetic and Cholinergic Influences on Cerebral Vasodilation Caused by Sciatic Nerve Stimulation in the Rat

Cited by 18 publications

References 30 publications

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

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

The Neurovascular Unit Coming of Age: A Journey through Neurovascular Coupling in Health and Disease

Competitive inhibition of nitric oxide synthase prevents the cortical hyperemia associated with peripheral nerve stimulation.

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