Neurochemical responses to chromatic and achromatic stimuli in the human visual cortex
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem
Grantová podpora
KL2 TR000113
NCATS NIH HHS - United States
UL1 TR000114
NCATS NIH HHS - United States
P30 NS076408
NINDS NIH HHS - United States
P41 EB015894
NIBIB NIH HHS - United States
PubMed
28273721
PubMed Central
PMC5951013
DOI
10.1177/0271678x17695291
Knihovny.cz E-zdroje
- Klíčová slova
- MR spectroscopy, energy metabolism, functional MRI, glutamate, lactate,
- MeSH
- barva * MeSH
- energetický metabolismus MeSH
- glukosa metabolismus MeSH
- kyselina asparagová metabolismus MeSH
- kyselina glutamová metabolismus MeSH
- kyselina mléčná metabolismus MeSH
- lidé MeSH
- magnetická rezonanční spektroskopie MeSH
- magnetická rezonanční tomografie MeSH
- mozek - chemie fyziologie MeSH
- neurony fyziologie MeSH
- oxidace-redukce MeSH
- respirační komplex IV metabolismus MeSH
- světelná stimulace * MeSH
- zdraví dobrovolníci pro lékařské studie MeSH
- zrakové evokované potenciály MeSH
- zrakové korové centrum metabolismus fyziologie MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- glukosa MeSH
- kyselina asparagová MeSH
- kyselina glutamová MeSH
- kyselina mléčná MeSH
- respirační komplex IV MeSH
In the present study, we aimed at determining the metabolic responses of the human visual cortex during the presentation of chromatic and achromatic stimuli, known to preferentially activate two separate clusters of neuronal populations (called "blobs" and "interblobs") with distinct sensitivity to color or luminance features. Since blobs and interblobs have different cytochrome-oxidase (COX) content and micro-vascularization level (i.e., different capacities for glucose oxidation), different functional metabolic responses during chromatic vs. achromatic stimuli may be expected. The stimuli were optimized to evoke a similar load of neuronal activation as measured by the bold oxygenation level dependent (BOLD) contrast. Metabolic responses were assessed using functional 1H MRS at 7 T in 12 subjects. During both chromatic and achromatic stimuli, we observed the typical increases in glutamate and lactate concentration, and decreases in aspartate and glucose concentration, that are indicative of increased glucose oxidation. However, within the detection sensitivity limits, we did not observe any difference between metabolic responses elicited by chromatic and achromatic stimuli. We conclude that the higher energy demands of activated blobs and interblobs are supported by similar increases in oxidative metabolism despite the different capacities of these neuronal populations.
CEITEC Central European Institute of Technology Masaryk University Brno Czech Republic
Division of Biostatistics School of Public Health University of Minnesota Minneapolis MN USA
Fondazione Santa Lucia IRCCS Rome Italy
MARBILab Museo storico della fisica e Centro di studi e ricerche Enrico Fermi Rome Italy
Physics Department University of Sao Paulo Ribeirao Preto SP Brazil
Zobrazit více v PubMed
Horton JC, Hedley-Whyte ET. Mapping of cytochrome oxidase patches and ocular dominance columns in human visual cortex. Philos Trans R Soc Lond B Biol Sci 1984; 304: 255–272. PubMed
Wong-Riley MT. Cytochrome oxidase: An endogenous metabolic marker for neuronal activity. Trends Neurosci 1989; 12: 94–101. PubMed
Zheng D, LaMantia AS, Purves D. Specialized vascularization of the primate visual cortex. J Neurosci 1991; 11: 2622–2629. PubMed PMC
Keller AL, Schuz A, Logothetis NK, et al. Vascularization of cytochrome oxidase-rich blobs in the primary visual cortex of squirrel and macaque monkeys. J Neurosci 2011; 31: 1246–1253. PubMed PMC
Borowsky IW, Collins RC. Metabolic anatomy of brain: A comparison of regional capillary density, glucose metabolism, and enzyme activities. J Comp Neurol 1989; 288: 401–413. PubMed
Lu HD, Roe AW. Functional organization of color domains in V1 and V2 of macaque monkey revealed by optical imaging. Cereb Cortex 2008; 18: 516–533. PubMed PMC
Tootell RB, Silverman MS, Hamilton SL, et al. Functional anatomy of macaque striate cortex. III. Color. J Neurosci 1988; 8: 1569–1593. PubMed PMC
Landisman CE, Ts'o DY. Color processing in macaque striate cortex: Electrophysiological properties. J Neurophysiol 2002; 87: 3138–3151. PubMed
Landisman CE, Ts'o DY. Color processing in macaque striate cortex: Relationships to ocular dominance, cytochrome oxidase, and orientation. J Neurophysiol 2002; 87: 3126–3137. PubMed
Mangia S, Tkac I, Gruetter R, et al. Sustained neuronal activation raises oxidative metabolism to a new steady-state level: Evidence from 1H NMR spectroscopy in the human visual cortex. J Cereb Blood Flow Metab 2007; 27: 1055–1063. PubMed
Lin Y, Stephenson MC, Xin L, et al. Investigating the metabolic changes due to visual stimulation using functional proton magnetic resonance spectroscopy at 7 T. J Cereb Blood Flow Metab 2012; 32: 1484–1495. PubMed PMC
Schaller B, Mekle R, Xin L, et al. Net increase of lactate and glutamate concentration in activated human visual cortex detected with magnetic resonance spectroscopy at 7 tesla. J Neurosci Res 2013; 91: 1076–1083. PubMed
Bednarik P, Tkac I, Giove F, et al. Neurochemical and BOLD responses during neuronal activation measured in the human visual cortex at 7 Tesla. J Cereb Blood Flow Metab 2015; 35: 601–610. PubMed PMC
Mangia S, Simpson IA, Vannucci SJ, et al. The in vivo neuron-to-astrocyte lactate shuttle in human brain: Evidence from modeling of measured lactate levels during visual stimulation. J Neurochem 2009; 109(Suppl 1): 55–62. PubMed PMC
DiNuzzo M, Mangia S, Maraviglia B, et al. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: Evidence from mathematical modeling. J Cereb Blood Flow Metab 2010; 30: 586–602. PubMed PMC
McKenna MC, Waagepetersen HS, Schousboe A, et al. Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: Current evidence and pharmacological tools. Biochem Pharmacol 2006; 71: 399–407. PubMed
Leontiev O, Buracas GT, Liang C, et al. Coupling of cerebral blood flow and oxygen metabolism is conserved for chromatic and luminance stimuli in human visual cortex. Neuroimage 2013; 68: 221–228. PubMed PMC
Buxton RB. Interpreting oxygenation-based neuroimaging signals: The importance and the challenge of understanding brain oxygen metabolism. Front Neuroenergetics 2010; 2: 8. PubMed PMC
Lee BB, Martin PR, Valberg A. The physiological basis of heterochromatic flicker photometry demonstrated in the ganglion cells of the macaque retina. J Physiol 1988; 404: 323–347. PubMed PMC
Oz G, Tkac I. Short-echo, single-shot, full-intensity proton magnetic resonance spectroscopy for neurochemical profiling at 4 T: Validation in the cerebellum and brainstem. Magn Reson Med 2011; 65: 901–910. PubMed PMC
Tkac I, Starcuk Z, Choi IY, et al. In vivo 1H NMR spectroscopy of rat brain at 1 ms echo time. Magn Reson Med 1999; 41: 649–656. PubMed
Gruetter R, Tkac I. Field mapping without reference scan using asymmetric echo-planar techniques. Magn Reson Med 2000; 43: 319–323. PubMed
Deelchand DK, Adanyeguh IM, Emir UE, et al. Two-site reproducibility of cerebellar and brainstem neurochemical profiles with short-echo, single-voxel MRS at 3T. Magn Reson Med 2015; 73: 1718–1725. PubMed PMC
Klose U. In vivo proton spectroscopy in presence of eddy currents. Magn Reson Med 1990; 14: 26–30. PubMed
Zhu XH, Chen W. Observed BOLD effects on cerebral metabolite resonances in human visual cortex during visual stimulation: A functional (1)H MRS study at 4 T. Magn Reson Med 2001; 46: 841–847. PubMed
Mangia S, Tkac I, Gruetter R, et al. Sensitivity of single-voxel 1H-MRS in investigating the metabolism of the activated human visual cortex at 7 T. Magn Reson Imaging 2006; 24: 343–348. PubMed
Emir UE, Raatz S, McPherson S, et al. Noninvasive quantification of ascorbate and glutathione concentration in the elderly human brain. NMR Biomed 2011; 24: 888–894. PubMed PMC
Liu X, Zhu XH, Chen W. Baseline BOLD correlation predicts individuals' stimulus-evoked BOLD responses. Neuroimage 2011; 54: 2278–2286. PubMed PMC
D'Esposito M, Deouell LY, Gazzaley A. Alterations in the BOLD fMRI signal with ageing and disease: A challenge for neuroimaging. Nat Rev Neurosci 2003; 4: 863–872. PubMed
Leontiev O, Buxton RB. Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI. Neuroimage 2007; 35: 175–184. PubMed PMC
Silver NC, Hittner JB, May K. Testing dependent correlations with nonoverlapping variables: A Monte Carlo simulation. Journal of Experimental Education 2004; 73: 53–69.
Mangia S, Giove F, Tkac I, et al. Metabolic and hemodynamic events after changes in neuronal activity: Current hypotheses, theoretical predictions and in vivo NMR experimental findings. J Cereb Blood Flow Metab 2009; 29: 441–463. PubMed PMC
Fox PT, Raichle ME, Mintun MA, et al. Nonoxidative glucose consumption during focal physiologic neural activity. Science 1988; 241: 462–464. PubMed
Terpstra M, Cheong I, Lyu T, et al. Test-retest reproducibility of neurochemical profiles with short-echo, single-voxel MR spectroscopy at 3T and 7T. Magn Reson Med 2016; 76: 1083–1091. PubMed PMC
Tkac I, Oz G, Adriany G, et al. In vivo 1H NMR spectroscopy of the human brain at high magnetic fields: Metabolite quantification at 4T vs. 7T. Magn Reson Med 2009; 62: 868–879. PubMed PMC
Mekle R, Mlynarik V, Gambarota G, et al. MR spectroscopy of the human brain with enhanced signal intensity at ultrashort echo times on a clinical platform at 3T and 7T. Magn Reson Med 2009; 61: 1279–1285. PubMed
Uludag K, Steinbrink J, Kohl-Bareis M, et al. Cytochrome-c-oxidase redox changes during visual stimulation measured by near-infrared spectroscopy cannot be explained by a mere cross talk artefact. Neuroimage 2004; 22: 109–119. PubMed
Wong-Riley MT. Bigenomic regulation of cytochrome c oxidase in neurons and the tight coupling between neuronal activity and energy metabolism. Adv Exp Med Biol 2012; 748: 283–304. PubMed PMC
Shapley R, Hawken MJ. Color in the cortex: Single- and double-opponent cells. Vision Res 2011; 51: 701–717. PubMed PMC
Livingstone M, Hubel D. Segregation of form, color, movement, and depth: Anatomy, physiology, and perception. Science 1988; 240: 740–749. PubMed
Sincich LC, Horton JC. The circuitry of V1 and V2: Integration of color, form, and motion. Annu Rev Neurosci 2005; 28: 303–326. PubMed
Johnson EN, Van Hooser SD, Fitzpatrick D. The representation of S-cone signals in primary visual cortex. J Neurosci 2010; 30: 10337–10350. PubMed PMC