Topology and Hemodynamics of the Cortical Cerebrovascular System

Hirsch, Sven; Reichold, Johannes; Schneider, Matthias; Székely, Gábor; Weber, Bruno

doi:10.1038/jcbfm.2012.39

Cited by 113 publications

(121 citation statements)

References 94 publications

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“…However, this notion is not supported by recent quantitative analyses of the cerebral cortical vasculature (Tsai et al 2009;Keller et al 2011;Hirsch et al 2012;Blinder et al 2013). Astrocytic networks, however, do seem to be organized according to neuronal functional units.…”

Section: Morphology Of Astrocytes and Their Role As Interface Cellsmentioning

confidence: 51%

The Astrocyte: Powerhouse and Recycling Center

Weber

Barros

2015

Cold Spring Harb Perspect Biol

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153

121

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Brain metabolism is characterized by fuel monodependence, high-energy expenditure, autonomy from the rest of body, local recycling, and marked division of labor between cell types. Although neurons spend most of the brain's energy on signaling, astrocytes bear the brunt of the metabolic load, controlling the composition of the interstitial fluid, supplying neurons with energy substrates and precursors for biosynthesis, and recycling neurotransmitters, oxidized scavengers, and other waste products. Outstanding questions in this field are the role of oligodendrocytes, the metabolic behavior of the different subtypes of astrocytes during development and disease, and the emerging notion that metabolism may participate directly in information processing. T he energy requirements of the central nervous system (CNS) are very high compared with those of other organs. Although the brain accounts for merely 2% of body weight, it receives 15% of cardiac output, and uses 20% of the oxygen and 25% of the glucose of the total body turnover (Magistretti 2008). A special microarchitecture has evolved to support this extreme need, in which glial cells play a central role (Fig. 1). The microvasculature consists of a complex and dense network of highly interconnected blood vessels (Weber et al. 2008;Blinder et al. 2013) to ensure adequate delivery of oxygen and glucose. Although oxygen diffuses freely into the parenchyma, glucose and other hydrophilic energy substrates are translocated across membranes via specific transporter proteins (Fig. 1). The astrocyte is a polarized cell. One set of astrocytic processes ensheaths the vasculature and a second set reaches toward the synapse, the site of highest energy demand (Harris et al. 2012). Much of the ATP produced in the brain is spent by neurons on the recovery of ion gradients challenged by postsynaptic potentials, with a smaller investment in action potentials and neurotransmitter recycling (Harris et al. 2012). Astrocytes consume considerable energy for their own needs and the cycling of metabolically relevant substances for neurons. These metabolic processes in astrocytes and neurons are the basis for brain mapping using functional magnetic resonance imaging and positron emission tomography (PET)-methods that capture local metabolism either directly or indirectly via hemodynamic changes (Magistretti 2008;Belanger et al. 2011a). Levels of energy consumption in the whole brain are almost constant. However, individual neurons can increase their consumption dramatically. For example, a striatal neuron may Overview of astrocytic metabolism. (Inset) Astrocytes (green) reside between blood vessels (red) and neurons (yellow). Neurons and oligodendrocytes (blue) are not in direct contact with vessels. Astrocytes form metabolic domains and are coupled by gap junctions, through which they exchange metabolites and ions. Energy: The main energy substrate of the brain is glucose (glc), which crosses the endothelium and enters astrocytes via the glucose transporter GLUT1. Glucose is converted b...

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Section: Morphology Of Astrocytes and Their Role As Interface Cellsmentioning

confidence: 51%

The Astrocyte: Powerhouse and Recycling Center

Weber

Barros

2015

Cold Spring Harb Perspect Biol

Self Cite

153

121

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“…The vascular network of the brain has unique structural features, aimed at preventing reductions in cerebral perfusion in response to vascular occlusion (22,34). At a large scale, redundancy is introduced at the level of the circle of Willis.…”

Section: Cerebral Vascular Anatomymentioning

confidence: 99%

Neurovascular Regulation in the Ischemic Brain

Jackman

Iadecola

2015

Antioxidants & Redox Signaling

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Significance: The brain has high energetic requirements and is therefore highly dependent on adequate cerebral blood supply. To compensate for dangerous fluctuations in cerebral perfusion, the circulation of the brain has evolved intrinsic safeguarding measures. Recent Advances and Critical Issues: The vascular network of the brain incorporates a high degree of redundancy, allowing the redirection and redistribution of blood flow in the event of vascular occlusion. Furthermore, active responses such as cerebral autoregulation, which acts to maintain constant cerebral blood flow in response to changing blood pressure, and functional hyperemia, which couples blood supply with synaptic activity, allow the brain to maintain adequate cerebral perfusion in the face of varying supply or demand. In the presence of stroke risk factors, such as hypertension and diabetes, these protective processes are impaired and the susceptibility of the brain to ischemic injury is increased. One potential mechanism for the increased injury is that collateral flow arising from the normally perfused brain and supplying blood flow to the ischemic region is suppressed, resulting in more severe ischemia. Future Directions: Approaches to support collateral flow may ameliorate the outcome of focal cerebral ischemia by rescuing cerebral perfusion in potentially viable regions of the ischemic territory.

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“…The analysis suggested that the vascular network is closely interconnected with the noncolumnar pattern of blood flow, which is contrary to the observations of Woolsey et al (1996) and makes the barrel-specific vascular model controversial. This issue was considered to be one of the most important questions in the field of vascular architecture analysis (Gardner 2010;Hirsch et al 2012). Moreover, Meyer et al (2010) raised another open question about whether the cellular and vascular architectures are similar across barrels.…”

Section: Introductionmentioning

confidence: 99%

“…The ability of functional brain imaging to distinguish the cortical columns relies heavily on whether the blood in these columns is supplied or drained by a specific vascular module, and a detailed investigation is needed to characterize the vascular distribution among cortical columns, preferably using direct 3D reconstruction and quantitative analysis (Gardner 2010;Hirsch et al 2012).…”

Section: Introductionmentioning

confidence: 99%

Direct 3D Analyses Reveal Barrel-Specific Vascular Distribution and Cross-Barrel Branching in the Mouse Barrel Cortex

Guo

Chen

et al. 2014

Cereb. Cortex

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Jingpeng Wu and Congdi Guo contributed equally to this work.Whether vascular distribution is spatially specific among cortical columns is a fundamental yet controversial question. Here, we have obtained 1-μm resolution 3D datasets that cover the whole mouse barrel cortex by combining Nissl staining with micro-optical sectioning tomography to simultaneously visualize individual cells and blood vessels, including capillaries. Pinpointing layer IV of the posteromedial barrel subfield, direct 3D reconstruction and quantitative analysis showed that (1) penetrating vessels preferentially locate in the interbarrel septa/barrel wall (75.1%) rather than the barrel hollows, (2) the branches of 70% penetrating vessels only reach the neighboring but not always all the neighboring barrels and the other 30% extend beyond the neighboring barrels and may provide cross-barrel blood supply or drainage, (3) the branches of 59.6% penetrating vessels reach all the neighboring barrels, while the rest only reach part of them, and (4) the length density of microvessels in the interbarrel septa/barrel wall is lower than that in the barrel hollows with a ratio of 0.92. These results reveal that the penetrating vessels and microvessels exhibit a barrel-specific organization, whereas the branches of penetrating vessels do not, which suggests a much more complex vascular distribution pattern among cortical columns than previously thought.

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Topology and Hemodynamics of the Cortical Cerebrovascular System

Cited by 113 publications

References 94 publications

The Astrocyte: Powerhouse and Recycling Center

The Astrocyte: Powerhouse and Recycling Center

Neurovascular Regulation in the Ischemic Brain

Direct 3D Analyses Reveal Barrel-Specific Vascular Distribution and Cross-Barrel Branching in the Mouse Barrel Cortex

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