Abstract
Theories of neurocognitive aging rely heavily on functional magnetic resonance imaging (fMRI) to test hypotheses regarding the brain basis of age-differences in cognition. This technique is based on the blood-oxygen level dependent signal (BOLD) that arises from the coordinated neural-vascular coupling that leads to increased blood flow following an increase in neural activity. Here we review the literature and current controversies regarding the mechanisms by which blood flow and neural activity are coupled, and how they change in the aging process. This literature suggests that neural-vascular coupling is a complex of processes, involving dynamic signaling between neurons, glia, and blood vessels. Nearly every component of this process is affected in aging leading to changes in BOLD and pervasive age-related cognitive changes.
Original language | English (US) |
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Pages (from-to) | 927-944 |
Number of pages | 18 |
Journal | Neuroscience and Biobehavioral Reviews |
Volume | 107 |
DOIs | |
State | Published - Dec 2019 |
Keywords
- Aging
- Cognition
- Cognitive aging
- Neurovascular coupling
- Processing speed
- fMRI
ASJC Scopus subject areas
- Neuropsychology and Physiological Psychology
- Cognitive Neuroscience
- Behavioral Neuroscience
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In: Neuroscience and Biobehavioral Reviews, Vol. 107, 12.2019, p. 927-944.
Research output: Contribution to journal › Review article › peer-review
}
TY - JOUR
T1 - A neural-vascular complex of age-related changes in the human brain
T2 - Anatomy, physiology, and implications for neurocognitive aging
AU - Abdelkarim, Dema
AU - Zhao, Yuguang
AU - Turner, Monroe P.
AU - Sivakolundu, Dinesh K.
AU - Lu, Hanzhang
AU - Rypma, Bart
N1 - Funding Information: This work was supported by NIH grant R01AG04797 (BR, HL). The authors would like to thank Eyad Alrabbat and Othman Elsehety for helpful input on early versions of this manuscript. Anaerobic glycolysis The rapid metabolism of glucose without oxygen to yield 2 ATP molecules Antigens Substances that bind to antibodies Antioxidants Substances that inhibit the production of or inactivate reactive oxygen species Apoptosis Programmed cell death Aquaporins Membrane proteins that allow for the transfer of water and soluble substances between cells Astrocyte-neuron lactate shuttle A process in which astrocytes supply neurons with lactate to metabolize Atherosclerosis The narrowing of an arterial lumen due to plaque buildup Blood-brain barrier A protective complex surrounding blood vessels in the brain made up of astrocyte endfeet and proteins that seal the vessel to prevent blood and other neurotoxic substances from leaking into brain tissue Calcium spreading When a cell situated within a network of similar cells encounters an increase in intracellular calcium, it signals this increase to other cells by sending calcium into the network Cerebral blood flow (CBF) The rate at which blood flows through the brain or a region of the brain Cerebral infarcts Instances of brain tissue death due to lack of blood flow to a region of the brain Cerebral metabolic rate of oxygen (CMRO 2 ) The rate at which the brain or a region of the brain consumes oxygen Cognitive efficiency The extent to which one performs cognitive operations quickly and accurately with the minimal effort or resources necessary, leading to optimal performance Complex I (NADH cytochrome c reductase) An enzyme in the electron transport chain critical for the metabolism of nicotinamide adenine dinucleotide in ATP production Complex IV (cytochrome c oxidase) An enzyme in the electron transport chain toward the end of the chain that receives electrons from upstream processes Cytokines Substances secreted by immune cells as part of an immune response Electron transport chain A series of enzyme complexes that transfer electrons to and from molecules to synthesize ATP Endothelial cells Cells that line the lumen of blood vessels Functional hyperemia The increase in blood flow following increases in neural activity Glucose A sugar molecule that is broken down by metabolic processes to produce energy for cells in the form of ATP Glycogen A compound comprised of multiple glucose molecules bound together for energy storage Glymphatic clearance The process by which metabolic byproducts are cleared from brain parenchyma Growth factors Substances that promote proliferation of cells and cellular structures Hemodynamic equivalence assumption The assumption that older and younger adults have equivalent vascular responses to neural stimuli Hemodynamic response function (HRF) The function that describes the time-course of BOLD signal change reflecting the vascular response to neural stimulation Hyperoxia A state of higher oxygen concentration than normally contained in room air Hyperpolarization When the neural membrane voltage becomes more negative, making it less likely for an action potential to fire Hypertrophy An increase in the size of a cell or group of cells Inflammation Signaling cascades that result from cellular damage Lactate A sugar molecule that pyruvate is converted to following glycolysis Lamellae Layers of myelin that form the myelin sheath Lumen The inner part of a blood vessel through which blood flows Microvascular lesioning Destruction of cellular structures that make up small blood vessels NAD+ (nicotinamide adenine dinucleotide) A coenzyme essential for oxidative metabolism that performs electron transfer reactions Neural efficiency The extent to which neurons perform achieve maximum performance with minimal energy expenditure Neural-vascular coupling The process by which neurons signal blood vessels, possibly via glia and other intermediaries, to dilate following an increase in neural activity Nitric oxide (NO) A signaling molecule and vasodilator Nitric oxide synthase (NOS) An enzyme that produces nitric oxide Oxidative phosphorylation The metabolism of glucose in the presence of oxygen into about 36 molecules of ATP Oxidative stress The unregulated production of reactive oxygen species by metabolic processes Progenitor cell A cell that has not yet differentiated into a cell of a specific type Prostaglandins Compounds with various signaling functions, including the dilation of vasculature Prostanoids A class of signaling molecules converted from arachidonic acid that are involved in inflammatory responses and vasoconstriction Protein nitration A reaction typically caused by oxidative stress that can alter protein function. Pyruvate A sugar molecule that is the product of glycolysis Reactive astrogliosis A state of heightened immunological and inflammatory signaling astrocytes enter in response to neuronal insult Reactive oxygen species (ROS) Volatile byproducts of oxidative metabolism that are highly unstable Sirtuins Signaling molecules with a highly diverse range of functions including regulation of cell death, aging, and inflammation Smooth muscle cells Cells that line the outside of arteries and arterioles that cause the lumen to dilate when they are relaxed and constrict when they contract Splitting and blebbing Separation and bubble formation between myelin lamellae Susceptibility effects Inhomogeneities in a standing magnetic field caused by magnetic properties of objects or materials within the field T2*-weighted signal An MRI contrast that takes advantage of the paramagnetic properties of deoxyhemoglobin to detect hemodynamic changes in the brain via blood oxygenation changes Transcription factors Proteins that regulate the synthesis of other proteins by controlling gene expression Vasoconstrictor A substance or stimulus that will cause a blood vessel to constrict and restrict blood flow Vasodilator A substance or stimulus that will cause a blood vessel to dilate and increase blood flow Vasomodulators Substances that interact with blood vessels and cause them to dilate or constrict Publisher Copyright: © 2019
PY - 2019/12
Y1 - 2019/12
N2 - Theories of neurocognitive aging rely heavily on functional magnetic resonance imaging (fMRI) to test hypotheses regarding the brain basis of age-differences in cognition. This technique is based on the blood-oxygen level dependent signal (BOLD) that arises from the coordinated neural-vascular coupling that leads to increased blood flow following an increase in neural activity. Here we review the literature and current controversies regarding the mechanisms by which blood flow and neural activity are coupled, and how they change in the aging process. This literature suggests that neural-vascular coupling is a complex of processes, involving dynamic signaling between neurons, glia, and blood vessels. Nearly every component of this process is affected in aging leading to changes in BOLD and pervasive age-related cognitive changes.
AB - Theories of neurocognitive aging rely heavily on functional magnetic resonance imaging (fMRI) to test hypotheses regarding the brain basis of age-differences in cognition. This technique is based on the blood-oxygen level dependent signal (BOLD) that arises from the coordinated neural-vascular coupling that leads to increased blood flow following an increase in neural activity. Here we review the literature and current controversies regarding the mechanisms by which blood flow and neural activity are coupled, and how they change in the aging process. This literature suggests that neural-vascular coupling is a complex of processes, involving dynamic signaling between neurons, glia, and blood vessels. Nearly every component of this process is affected in aging leading to changes in BOLD and pervasive age-related cognitive changes.
KW - Aging
KW - Cognition
KW - Cognitive aging
KW - Neurovascular coupling
KW - Processing speed
KW - fMRI
UR - http://www.scopus.com/inward/record.url?scp=85074412855&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85074412855&partnerID=8YFLogxK
U2 - 10.1016/j.neubiorev.2019.09.005
DO - 10.1016/j.neubiorev.2019.09.005
M3 - Review article
C2 - 31499083
AN - SCOPUS:85074412855
SN - 0149-7634
VL - 107
SP - 927
EP - 944
JO - Neuroscience and Biobehavioral Reviews
JF - Neuroscience and Biobehavioral Reviews
ER -