Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina

Riva, Charles E.; Logean, Eric; Falsini, Benedetto

doi:10.1016/j.preteyeres.2004.07.002

Cited by 235 publications

(213 citation statements)

References 85 publications

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“…Experiments were conducted on the acutely isolated mammalian retina. As in the brain, neuronal activity in the retina evokes increases in blood flow (Riva et al, 2005). We found that both light stimulation and glial cell stimulation evoked vasomotor responses in retinal arterioles.…”

Section: Introductionmentioning

confidence: 61%

Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling

Metea¹,

Newman²

2006

J. Neurosci.

551

584

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Neuronal activity evokes localized changes in blood flow. Although this response, termed neurovascular coupling, is widely used to monitor human brain function and diagnose pathology, the cellular mechanisms that mediate the response remain unclear. We investigated the contribution of glial cells to neurovascular coupling in the acutely isolated mammalian retina. We found that light stimulation and glial cell stimulation can both evoke dilation or constriction of arterioles. Light-evoked and glial-evoked vasodilations were blocked by inhibitors of cytochrome P450 epoxygenase, the synthetic enzyme for epoxyeicosatrienoic acids. Vasoconstrictions, in contrast, were blocked by an inhibitor of -hydroxylase, which synthesizes 20-hydroxyeicosatetraenoic acid. Nitric oxide influenced whether vasodilations or vasoconstrictions were produced in response to light and glial stimulation. Light-evoked vasoactivity was blocked when neuron-to-glia signaling was interrupted by a purinergic antagonist. These results indicate that glial cells contribute to neurovascular coupling and suggest that regulation of blood flow may involve both vasodilating and vasoconstricting components.

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Section: Introductionmentioning

confidence: 61%

Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling

Metea¹,

Newman²

2006

J. Neurosci.

551

584

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“…16,17 When the retina is stimulated by a flickering light, blood flow in the retinal vasculature increases significantly. 18 This increase in blood flow, the functional hyperemia response, supplies oxygen and glucose to the active neurons in the inner and middle retinal layers. This hemodynamic response is present in the cerebral circulation as well and was described long ago in the cerebral cortex by Mosso 19 and Roy and Sherrington.…”

Section: Introductionmentioning

confidence: 99%

Functional Hyperemia and Mechanisms of Neurovascular Coupling in the Retinal Vasculature

Newman

2013

J Cereb Blood Flow Metab

191

162

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The retinal vasculature supplies cells of the inner and middle layers of the retina with oxygen and nutrients. Photic stimulation dilates retinal arterioles producing blood flow increases, a response termed functional hyperemia. Despite recent advances, the neurovascular coupling mechanisms mediating the functional hyperemia response in the retina remain unclear. In this review, the retinal functional hyperemia response is described, and the cellular mechanisms that may mediate the response are assessed. These neurovascular coupling mechanisms include neuronal stimulation of glial cells, leading to the release of vasoactive arachidonic acid metabolites onto blood vessels, release of potassium from glial cells onto vessels, and production and release of nitric oxide (NO), lactate, and adenosine from neurons and glia. The modulation of neurovascular coupling by oxygen and NO are described, and changes in functional hyperemia that occur with aging and in diabetic retinopathy, glaucoma, and other pathologies, are reviewed. Finally, outstanding questions concerning retinal blood flow in health and disease are discussed. In lower vertebrates that have thinner retinas, including amphibians, reptiles, and some mammals, the retinal vasculature is absent and the choroidal circulation supplies the entire retina. 2 The choroidal circulation is supplied by the long and short ciliary arteries and the anterior ciliary arteries, which feed the large arteries in the outer portion of the choroid. 3 These arteries branch into smaller vessels, which, in turn, feed the highly anastomosed choriocapillaris network lying at the inner border of the choroid, adjacent to the retinal pigment epithelium and retinal photoreceptors. The total blood flow supplying the choroid is much greater than that supplying the retina (606 vs. 25 mg/min/ whole tissue 4 ), to meet the high metabolic demands of the photoreceptors. 5 The retinal vasculature is supplied by the central retinal artery, which enters the retina with the optic nerve at the optic disc. The artery branches into radial arterioles and smaller vessels on the vitreal surface of the retina. 3 Pre-capillary arterioles and capillaries ramify from these surface vessels and form anastomotic networks in the ganglion cell layer, just beneath the retinal surface, and deeper in the inner nuclear layer, supplying horizontal cells, bipolar cells, amacrine cells, and Mü ller glial cells. Blood is returned through radial venules on the retinal surface that empty into the central retinal vein in the optic nerve. Journal of Cerebral BloodThe retinal and choroidal vasculatures differ in several respects. Retinal vessels lack autonomic innervation, 6,7 whereas the choroidal circulation is innervated by both sympathetic and parasympathetic

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“…Blood flow in the retina is tightly regulated and intricately coupled to basal metabolic function under normal physiological conditions (Riva et al, 2005). Perturbations of basal blood flow and its coupling to metabolic function have been implicated in many retinal diseases, such as retinal ischemia and diabetic retinopathy, which could lead to acute or gradual loss of vision.…”

Section: Introductionmentioning

confidence: 99%

“…Blood flow in the retina has been studied using microsphere techniques (Wang et al, 2007), fluorescein angiography (Preussner et al, 1983), indocyanin-green angiography (Guyer et al, 1993), laser Doppler flowmetry (LDF) (Formaz et al, 1997), and laser speckle imaging (Cheng and Duong, 2007) (reviewed in Riva et al, 2005). These techniques have made remarkable contributions to our understanding of normal retinal physiology and pathophysiology.…”

Section: Introductionmentioning

confidence: 99%

Blood-flow magnetic resonance imaging of the retina

Cheng

Duong

2008

NeuroImage

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This study describes a novel MRI application to image basal blood flow, physiologically induced blood-flow changes, and the effects of isoflurane concentration on blood flow in the retina. Continuous arterial-spin-labeling technique with a separate neck coil for spin labeling was used to image blood flow of the rat retina at 90×90×1500-μm resolution. The average blood flow of the whole retina was 6.3±1.0 ml/g/min under 1% isoflurane, consistent with the high blood flow in the retina reported using other techniques. Blood flow is relatively constant along the length of the retina, except it dipped slightly around the optic nerve head and dropped significantly at the distal edges where the retina terminates. Hyperoxia (100% O 2 ) decreased blood flow 25± 6% relative to baseline (air) due to vasoconstriction. Hypercapnia (5% CO 2 +21% O 2 ) increased blood flow 16±6% due to vasodilation. Increasing isoflurane (a potent vasodilator) concentration to 1.5% increased blood flow to 9.3±2.7 ml/g/min. Blood-flow signals were confirmed to be genuine by repeating measurements after the animals were sacrificed in the MRI scanner. This study demonstrates a proof of concept that quantitative blood flow of the retina can be measured using MRI without depth limitation. Bloodflow MRI has the potential to provide unique insights into retinal physiology, serve as an early biomarker for some retinal diseases, and could complement optically based imaging techniques.

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Visually evoked hemodynamical response and assessment of neurovascular coupling in the optic nerve and retina

Cited by 235 publications

References 85 publications

Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling

Glial Cells Dilate and Constrict Blood Vessels: A Mechanism of Neurovascular Coupling

Functional Hyperemia and Mechanisms of Neurovascular Coupling in the Retinal Vasculature

Blood-flow magnetic resonance imaging of the retina

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