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      Neural Mechanisms of Age-Related Slowing: The ΔCBF/ΔCMRO 2 Ratio Mediates Age-Differences in BOLD Signal and Human Performance

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          Abstract

          The precise mechanisms that give rise to the blood-oxygen-level-dependent (BOLD) activation differences that accompany age-related cognitive slowing remain fundamentally unknown. We sought to isolate the origin of age-related BOLD changes by comparing blood-flow and oxygen-metabolic constituents of the BOLD response using dual-echo arterial spin labeling during visual stimulation and CO 2 ingestion. We hypothesized, and our results confirmed, that age-related changes in the ratio of fractional cerebral blood flow to fractional cerebral metabolic rate of oxygen consumption (ΔCBF/ΔCMRO 2) lead to the BOLD changes that are observed in older adults. ΔCBF/ΔCMRO 2 was also significantly related to performance, suggesting that age-related cognitive slowing results from neural cell assemblies that operate less efficiently, requiring greater oxygen metabolism that is not matched by blood-flow changes relative to younger adults. Age-related changes in ΔCBF/ΔCMRO 2 are sufficient to explain variations in BOLD responding and performance cited throughout the literature, assuming no bias based on physiological baseline CMRO 2.

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          Hemispheric asymmetry reduction in older adults: the HAROLD model.

          Roberto Cabeza (2002)
          A model of the effects of aging on brain activity during cognitive performance is introduced. The model is called HAROLD (hemispheric asymmetry reduction in older adults), and it states that, under similar circumstances, prefrontal activity during cognitive performances tends to be less lateralized in older adults than in younger adults. The model is supported by functional neuroimaging and other evidence in the domains of episodic memory, semantic memory, working memory, perception, and inhibitory control. Age-related hemispheric asymmetry reductions may have a compensatory function or they may reflect a dedifferentiation process. They may have a cognitive or neural origin, and they may reflect regional or network mechanisms. The HAROLD model is a cognitive neuroscience model that integrates ideas and findings from psychology and neuroscience of aging.
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            Modeling the hemodynamic response to brain activation.

            Richard B. Buxton, Kâmil Uludağ, David J Dubowitz … (2004)
            Neural activity in the brain is accompanied by changes in cerebral blood flow (CBF) and blood oxygenation that are detectable with functional magnetic resonance imaging (fMRI) techniques. In this paper, recent mathematical models of this hemodynamic response are reviewed and integrated. Models are described for: (1) the blood oxygenation level dependent (BOLD) signal as a function of changes in cerebral oxygen extraction fraction (E) and cerebral blood volume (CBV); (2) the balloon model, proposed to describe the transient dynamics of CBV and deoxy-hemoglobin (Hb) and how they affect the BOLD signal; (3) neurovascular coupling, relating the responses in CBF and cerebral metabolic rate of oxygen (CMRO(2)) to the neural activity response; and (4) a simple model for the temporal nonlinearity of the neural response itself. These models are integrated into a mathematical framework describing the steps linking a stimulus to the measured BOLD and CBF responses. Experimental results examining transient features of the BOLD response (post-stimulus undershoot and initial dip), nonlinearities of the hemodynamic response, and the role of the physiologic baseline state in altering the BOLD signal are discussed in the context of the proposed models. Quantitative modeling of the hemodynamic response, when combined with experimental data measuring both the BOLD and CBF responses, makes possible a more specific and quantitative assessment of brain physiology than is possible with standard BOLD imaging alone. This approach has the potential to enhance numerous studies of brain function in development, health, and disease.
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              Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging.

              S Ogawa, D Tank, R. Menon … (1992)
              We report that visual stimulation produces an easily detectable (5-20%) transient increase in the intensity of water proton magnetic resonance signals in human primary visual cortex in gradient echo images at 4-T magnetic-field strength. The observed changes predominantly occur in areas containing gray matter and can be used to produce high-spatial-resolution functional brain maps in humans. Reducing the image-acquisition echo time from 40 msec to 8 msec reduces the amplitude of the fractional signal change, suggesting that it is produced by a change in apparent transverse relaxation time T*2. The amplitude, sign, and echo-time dependence of these intrinsic signal changes are consistent with the idea that neural activation increases regional cerebral blood flow and concomitantly increases venous-blood oxygenation.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Cereb Cortex
                Journal ID (iso-abbrev): Cereb. Cortex
                Journal ID (publisher-id): cercor
                Journal ID (hwp): cercor
                Title: Cerebral Cortex (New York, NY)
                Publisher: Oxford University Press
                ISSN (Print): 1047-3211
                ISSN (Electronic): 1460-2199
                Publication date (Print): October 2013
                Publication date (Electronic): 8 August 2012
                Publication date PMC-release: 8 August 2012
                Volume: 23
                Issue: 10
                Pages: 2337-2346
                Affiliations
                [1 ]School of Behavioral and Brain Sciences, University of Texas at Dallas , Richardson, TX 75080, USA,
                [2 ]Department of Psychiatry, University of Texas Southwestern Medical Center , Dallas, TX 75390, USA and
                [3 ]Advanced Imaging Research Center and Department of Radiology, University of Texas Southwestern Medical Center , Dallas, TX 75390, USA
                Author notes
                Address correspondence to J.L. Hutchison, Center for Brain Health, University of Texas at Dallas, 2200 W. Mockingbird Lane, Dallas, TX 75235, USA. Email: joanna.hutchison@ 123456utdallas.edu .
                Article
                Publisher ID: bhs233
                DOI: 10.1093/cercor/bhs233
                PMC ID: 3767961
                PubMed ID: 22879349
                SO-VID: 709a519c-5e95-4d02-9e10-5b719a9d6272
                Copyright © © The Author 2012. Published by Oxford University Press.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( http://creativecommons.org/licenses/by-nc/3.0), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Subject: Articles

                ScienceOpen disciplines: Neurology
                Keywords: aging,bold,cbf,cmro2,dual-echo asl,hypercapnia,neural efficiency,processing efficiency
                Data availability:
                ScienceOpen disciplines: Neurology
                Keywords: aging, bold, cbf, cmro2, dual-echo asl, hypercapnia, neural efficiency, processing efficiency

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