Where in-vivo imaging meets cytoarchitectonics: The relationship between cortical thickness and neuronal density measured with high-resolution [18F]flumazenil-PET

Fougère, Christian la; Grant, Sarah; Kostikov, Alexey; Schirrmacher, Ralf; Gravel, Paul; Schipper, Hyman M.; Reader, Andrew J.; Evans, Alan C.; Thiel, Alexander

doi:10.1016/j.neuroimage.2010.11.015

Cited by 122 publications

(95 citation statements)

References 55 publications

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“…From equation (3), it is important to note that regional variations of V ATP must be determined from quantitative CMR glc and CMR O2 data. Here, we found V ATP calculated from quantitative PET measurements in young healthy brain to be in good agreement with absolute V ATP measured by 31 P and 13 C magnetic resonance spectroscopy (MRS). [10][11][12][13] Regardless of size, spatial coordinates, or origin of the extended RfMRI-networks that we examined, the regional distributions revealed remarkably similar OEF and OGI values that were comparable in magnitude to gray matter means.…”

Section: Introductionsupporting

confidence: 75%

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Hyder

Hermán

Bailey

et al. 2016

J Cereb Blood Flow Metab

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Regionally variable rates of aerobic glycolysis in brain networks identified by resting-state functional magnetic resonance imaging (R-fMRI) imply regionally variable adenosine triphosphate (ATP) regeneration. When regional glucose utilization is not matched to oxygen delivery, affected regions have correspondingly variable rates of ATP and lactate production. We tested the extent to which aerobic glycolysis and oxidative phosphorylation power R-fMRI networks by measuring quantitative differences between the oxygen to glucose index (OGI) and the oxygen extraction fraction (OEF) as measured by positron emission tomography (PET) in normal human brain (resting awake, eyes closed). Regionally uniform and correlated OEF and OGI estimates prevailed, with network values that matched the gray matter means, regardless of size, location, and origin. The spatial agreement between oxygen delivery (OEF&0.4) and glucose oxidation (OGI & 5.3) suggests that no specific regions have preferentially high aerobic glycolysis and low oxidative phosphorylation rates, with globally optimal maximum ATP turnover rates (V ATP & 9.4 mmol/g/min), in good agreement with 31 P and 13 C magnetic resonance spectroscopy measurements. These results imply that the intrinsic network activity in healthy human brain powers the entire gray matter with ubiquitously high rates of glucose oxidation. Reports of departures from normal brain-wide homogeny of oxygen extraction fraction and oxygen to glucose index may be due to normalization artefacts from relative PET measurements.

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Section: Introductionsupporting

confidence: 75%

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Hyder

Hermán

Bailey

et al. 2016

J Cereb Blood Flow Metab

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“…This conclusion does not make any claims about uniformity of cellular density because the measured metabolic data from PET are susceptible to partial volume effects arising from either white matter or varying cortical thickness across the entire brain. 77 We made no attempt to apply any partial volume corrections based on the cortical thickness alone, which would presumably reduce the heterogeneity of metabolic values across regions even further. Until individual voxel PET and MRI data are available on an individual subject basis, partial volume effects of gray versus white matter cannot be quantitatively addressed.…”

Section: Discussionmentioning

confidence: 99%

“…The use of small average metabolic differences across regions as evidence that some networks have greater functional importance than others (e.g., default mode network [42][43][44] does not seem justified given the much larger underlying activity that all networks and regions share. However, future studies with better spatial resolution are needed to resolve white-matter partial volume effects to represent metabolism in gray matter, especially across the cerebral cortex where graymatter thickness varies considerably, 77 such that regional differences can be more quantitatively assessed. The dependence of task-induced response on the resting brain activity strongly argues for the functional relevance of high metabolic demand of the resting awake state.…”

Section: Discussionmentioning

confidence: 99%

Glutamatergic Function in the Resting Awake Human Brain is Supported by Uniformly High Oxidative Energy

Hyder

Fulbright

Shulman

et al. 2013

J Cereb Blood Flow Metab

107

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Rodent 13 C magnetic resonance spectroscopy studies show that glutamatergic signaling requires high oxidative energy in the awake resting state and allowed calibration of functional magnetic resonance imaging (fMRI) signal in terms of energy relative to the resting energy. Here, we derived energy used for glutamatergic signaling in the awake resting human. We analyzed human data of electroencephalography (EEG), positron emission tomography (PET) maps of oxygen (CMR O2 ) and glucose (CMR glc ) utilization, and calibrated fMRI from a variety of experimental conditions. CMR glc and EEG in the visual cortex were tightly coupled over several conditions, showing that the oxidative demand for signaling was four times greater than the demand for nonsignaling events in the awake state. Variations of CMR O2 and CMR glc from gray-matter regions and networks were within ±10% of means, suggesting that most areas required similar energy for ubiquitously high resting activity. Human calibrated fMRI results suggest that changes of fMRI signal in cognitive studies contribute at most ± 10% CMR O2 changes from rest. The PET data of sleep, vegetative state, and anesthesia show metabolic reductions from rest, uniformly 420% across, indicating no region is selectively reduced when consciousness is lost. Future clinical investigations will benefit from using quantitative metabolic measures. Keywords: astrocytes; baseline; field potentials; glutamate; multiunit activity; resting state INTRODUCTIONThe human brain consumes 20% of the body's energy at rest despite being only 2% of total body mass. 1 Normally glucose oxidation is the source of energy production supporting brain function 2 in which gray-matter signaling (i.e., events associated with neuronal firing) is dominated by glutamatergic neurons. 3 Estimates of the fraction of resting brain energy devoted to signaling were originally quite low. 4 But recent experimental studies in rodents and theoretical modeling have converged on the conclusion that majority of the resting energy consumption supports glutamatergic signaling and the energy demand changes linearly with pyramidal neuron firing rates and glutamate neurotransmitter release and reuptake. [5][6][7][8][9] Therefore in rodent models it is possible, to a first order, to show that the resting energy is primarily dedicated to total glutamatergic signaling, and the changes in neuronal signaling relative to a well-defined resting activity level can be used to calibrate changes in energy consumption during functional magnetic resonance imaging (fMRI) experiments. 10,11 In the awake human brain, however, the fraction of resting energy usage devoted to glutamatergic signaling is less well understood. The magnitude of neuronal signaling in the human brain, and by inference the commensurate energy demand, underscores the functional relevance of resting activity and has profound implications for interpreting fMRI experiments in humans. [12][13][14] Given the rapidly increasing use of resting-state fMRI in mapping networks-defined as a...

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“…In vivo MR imaging measurements have shown regional differences in cortical thickness (22) and have revealed focal differences in cortical thickness between healthy control subjects and patients with schizophrenia (23,24), Alzheimer disease (25) or autism (26). The ability to distinguish multiple cortical layers might yield more insight into where cortical thinning mainly takes place, be it in the superficial or deep layers or diffuse in all layers.…”

Section: Discussionmentioning

confidence: 99%

Generalized Multiple-Layer Appearance of the Cerebral Cortex with 3D FLAIR 7.0-T MR Imaging

Zwanenburg¹,

Hendrikse²,

Luijten³

2012

Radiology

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Where in-vivo imaging meets cytoarchitectonics: The relationship between cortical thickness and neuronal density measured with high-resolution [18F]flumazenil-PET

Cited by 122 publications

References 55 publications

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Uniform distributions of glucose oxidation and oxygen extraction in gray matter of normal human brain: No evidence of regional differences of aerobic glycolysis

Glutamatergic Function in the Resting Awake Human Brain is Supported by Uniformly High Oxidative Energy

Generalized Multiple-Layer Appearance of the Cerebral Cortex with 3D FLAIR 7.0-T MR Imaging

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