Vascularization of Cytochrome Oxidase-Rich Blobs in the Primary Visual Cortex of Squirrel and Macaque Monkeys

Keller, Anna Lena; Schüz, Almut; Logothetis, Nikos K.; Weber, Bruno

doi:10.1523/jneurosci.2765-10.2011

Cited by 42 publications

(36 citation statements)

References 49 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…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: 88%

The Astrocyte: Powerhouse and Recycling Center

Weber

Barros

2015

Cold Spring Harb Perspect Biol

153

121

View full text Add to dashboard Cite

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...

show abstract

Section: Morphology Of Astrocytes and Their Role As Interface Cellsmentioning

confidence: 88%

The Astrocyte: Powerhouse and Recycling Center

Weber

Barros

2015

Cold Spring Harb Perspect Biol

153

121

View full text Add to dashboard Cite

show abstract

“…The ascending thalamocortical input from the ventral posterior medial nucleus clustered in the barrel hollows and formed a cluster of synapses (Logothetis and Pfeuffer 2004), which is highly energy demanding (Attwell and Laughlin 2001). Interestingly, similar vascular distribution patterns were also observed among the blobs of the visual cortex in both the squirrel monkey brain (Zheng et al 1991) and the macaque brain (Keller et al 2011). Thus, the columnar distribution pattern of big penetrating vessels and capillaries may potentially be common among the cortical columns of mammalian brains.…”

Section: Discussionmentioning

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

View full text Add to dashboard Cite

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.

show abstract

“…Oxygen and glucose are delivered from the blood to active neurons through capillaries that cover the whole brain. Thus, capillary density correlates well with the demand for oxidative metabolism, as is identified by 2-deoxyglucose (2-DG) and cytochrome oxidase (Borowsky and Collins, 1989;Keller et al, 2011;Weber et al, 2008;Zheng et al, 1991). The average distance from a neuron to the nearest microvessel (defined as having a 3.5-4.0 mm diameter) is only $13 mm in the cerebral cortex (Tsai et al, 2009), which is, theoretically, the finest resolution fMRI can achieve to accurately represent neuronal activity.…”

Section: Vascular Constraintsmentioning

confidence: 96%