The metabolism of neurons and astrocytes through mathematical models

Annals of Biomedical Engineering

Volumn 40, Issue 11, 2012, Pages 2328-2344

  Somersalo, E ^a   Cheng, Y ^a   Calvetti, D ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Energy metabolism; Mathematical modeling; Probabilistic approach

Indexed keywords

BRAIN CELLS; BRAIN METABOLISM; ENERGY METABOLISM; IMAGING MODALITY; INTRINSIC VARIABILITIES; METABOLIC SYSTEMS; MODEL PARAMETERS; PROBABILISTIC APPROACHES;

BRAIN MODELS; FORECASTING; MATHEMATICAL MODELS; PHYSIOLOGY; PROBABILITY DISTRIBUTIONS;

METABOLISM;

ASTROCYTE; BIOLOGICAL MODEL; BRAIN; ENERGY METABOLISM; HUMAN; METABOLISM; NERVE CELL; REVIEW;

ASTROCYTES; BRAIN; ENERGY METABOLISM; HUMANS; MODELS, NEUROLOGICAL; NEURONS;

EID: 84868369392     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-012-0643-z     Document Type: Article

References (57)

1. Attwell, D., and S. B. Laughlin. An energy budget for signaling in the grey matter of the brain. J. Cereb. Blood Flow Metab. 21:1133-1145, 2001.
2. Aubert, A., and R. Costalat. A model of the coupling between brain electrical activity, metabolism, and hemodynamics: application to the interpretation of functional neuroimaging. NeuroImage 17:1162-1181, 2002.
3. Aubert, A., and R. Costalat. Interaction between astrocytes and neurons studied using a mathematical model of compartmentalized energy metabolism. J. Cereb. Blood Flow Metab. 25:1476-1490, 2005.
4. Aubert, A., R. Costalat, P. J. Magistretti, and L. Pellerin. Brain lactate kinetics: modeling evidence for neuronal lactate uptake upon activation. Proc. Natl Acad. Sci. U.S.A. 102:16448-16453, 2005.
5. Aubert, A., R. Costalat, and R. Valabrègue. Modelling of the coupling between brain electrical activity and metabolism. Acta. Biotheor. 49:301-326, 2001.
6. Bergersen, L. H., and A. Gjedde. Is lactate a volume transmitter of metabolic states of the brain? Front. Neuroenergetics 4:5, 2012.
7. Calvetti, D., R. Occhipinti, and E. Somersalo. The inverse problem of brain energetics: ketone bodies as alternative substrates. Proceedings of the applied inverse problems 2007: theoretical and computational aspects. J. Phys. Conf. Ser. 124:012013, 2008.
8. Calvetti, D., and E. Somersalo. Large scale statistical parameter estimation in complex systems with an application to metabolic models. Multiscale Model. Simul. 5:1333-1366, 2006.
9. Calvetti, D., and E. Somersalo. Introduction to Bayesian Scientific Computing - Ten Lectures on Subjective Computing. New York: Springer, 2007.
10. Calvetti, D., and E. Somersalo. Dynamic activation model for a glutamatergic neurovascular unit. J. Theor. Biol. 274:12-29, 2010.
11. Calvetti, D., and E. Somersalo. Me'nage à trois: the role of neurotransmitters in the energy metabolism of astrocytes, glutamatergic and GABAergic neurons. J. Cereb. Blood Flow Metab. 32:1472-1483, 2012.
12. Chih, C. P., and E. L. Roberts, Jr. Energy substrates for neurons during neural activity: a critical review of the astrocyte-neuron lactate shuttle hypothesis. J. Cereb. Blood Flow Metab. 23:1263-1281, 2003.
13. Cloutier, M., F. B. Bolger, and J. P. Lowry. An integrative dynamic model of brain energy metabolism using in vivo neurochemical measurement. J. Comput. Neurosci. 27:391-414, 2009.
14. Dash, R. K., Y. Li, J. Kim, G. M. Saidel, and M. E. Cabrera. Modeling cellular metabolism and energetics in skeletal muscle: large-scale parameter estimation and sensitivity analysis. IEEE Trans. Biomed. Eng. 55:1298-1318, 2008.
15. Dienel, G. Brain lactate metabolism: the discoveries and controversies. J. Cereb. Blood Flow Metab. 32:1107-1138, 2011.
16. DiNuzzo, M., S. Mangia, B. Maraviglia, and F. Giove. Changes in glucose uptake rather than lactate shuttle take center stage in subserving neuroenergetics: evidence from mathematical modeling. J. Cereb. Blood Flow Metab. 30:586-602, 2010.
17. Fillenz, M. The role of lactate in brain metabolism. Neurochem. Int. 47:413-417, 2005.
18. Fox, P. T., and M. E. Raichle. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl Acad. Sci. U.S.A. 83:1140-1144, 1986.
19. Fox, P. T., M. E. Raichle, M. A. Mintun, and C. Dence. Nonoxidative glucose consumption during focal physiologic neural activity. Science 241:462-464, 1988.
20. Gjedde, A. Rapid steady-state analysis of blood-brain glucose transfer in the rat. Acta Physiol. Scand. 108:331-339, 1980.
21. Gjedde, A. The relation between brain function and cerebral blood flow and metabolism. In: Cerebrovascular Disease, edited by H. H. Batjer. Philadelphia: Lippincott-Raven, 1997, pp. 23-40.
22. Gjedde, A. Coupling of brain function to metabolism: evaluation of energy requirements. In: Handbook of Neurochemistry and Molecular Neurobiology3rd, edited by A. Lajtha. Berlin: Springer, 2007.
23. Gjedde, A., and S. Marrett. Glycolysis in neurons, not astrocytes, delays oxidative metabolism of human visual cortex during sustained checkerboard stimulation in vivo. J. Cereb. Blood Flow Metab. 21:1384-1392, 2001.
24. Gjedde, A., S. Marrett, and M. Vafaee. Oxidative and nonoxidative metabolism of excited neurons and astrocytes. J. Cereb. Blood Flow Metab. 22:1-14, 2002.
25. Gruetter, R., E. R. Seaquist, and K. Ugurbil. A mathematical model of compartmentalized neurotransmitter metabolism in the human brain. Am. J. Physiol. Endocrinol. Metab. 281:E100-E112, 2001.
26. Heino, J., D. Calvetti, and E. Somersalo. Metabolica: a statistical research tool for analyzing metabolic networks. Comput. Methods Programs Biomed. 97:151-167, 2010.
27. Heinrich, R., and S. Schuster. The Regulation of Cellular Systems. New York: ITP Chapman & Hall, 1996.
28. Hertz, L. The astrocyte-neuron lactate shuttle: a challenge of a challenge. J. Cereb. Blood Flow Metab. 24:1241-1248, 2004.
29. Hertz, L. Brain glutamine synthesis requires neuronal aspartate: a commentary. J. Cereb. Blood Flow Metab. 31:384-387, 2011.
30. Hertz, L., L. Peng, and G. A. Dienel. Energy metabolism in astrocytes: high rate of oxidative metabolism and spatiotemporal dependence on glycolysis/glycogenolysis. J. Cereb. Blood Flow Metab. 27:219-249, 2007.
31. Hyder, F., A. B. Patel, A. Gjedde, D. L. Rothman, K. L. Behar, and R. G. Shulman. Neuronal-glial glucose oxidation and glutamatergic-GABAergic function. J. Cereb. Blood Flow Metab. 26:865-877, 2006.
32. Ivanov, K. P., Yu. Ya. Kislayokov, and M. O. Samoilov. Microcirculation and transport of oxygen to neurons of the brain. Microvasc. Res. 18:434-441, 1979.
33. Jolivet, R., I. Allaman, L. Pellerin, P. J. Magistretti, and B. Weber. Comment on recent modeling studies of astrocyte-neuron metabolic interactions. J. Cereb. Blood Flow Metab. 30:1982-1986, 2010.
34. Kasischke, K. A., H. D. Vishwasrao, P. J. Fisher, W. R. Zipfel, and W. W. Webb. Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305:99-103, 2004.
35. Kauffman, K. J., P. Prakesh, and J. S. Edwards. Advance in flux balance analysis. Curr. Opin. Biotechnol. 14:491-496, 2003.
36. Kemp, G. J. Non-invasive methods for studying brain energy metabolism: what they show and what it means. Dev. Neurosci. 22:418-428, 2000.
37. Krogh, A. The number and distribution of capillaries in muscles with calculations of the oxygen pressure head necessary for supplying the tissue. J. Physiol. 52:409-415, 1919.
38. LaNoue, K. F., V. Carson, D. A. Berkich, and S. M. Hutson. Mitochondrial/cytosolic interactions via metabolite shuttles and transporters. In: Handbook of Neurochemistry and Molecular Neurobiology. Brain Energetics. Integration of Molecular and Cellular Processes. Part VI, Chapter 1. Berlin: Springer, pp. 589-616, 2007.
39. Lovatt, D., U. Sonnewald, H. S. Waagepetersen, A. Schousboe, W. He, J. H. Lin, X. Han, T. Takano, S. Wang, F. J. Sim, S. A. Goldman, and M. Nedergaard. The transcriptome and metabolic gene signature of protoplasmic astrocytes in the adult murine cortex. J. Neurosci. 27:12255-12266, 2007.
40. Mangia, S., M. DiNuzzo, F. Giove, A. Carruthers, I. A. Simpson, and S. J. Vannucci. Response to 'comment on recent modeling studies of astrocyte-neuron metabolic interactions': much ado about nothing. J. Cereb. Blood Flow Metab. 31:1346-1353, 2011.
41. Mangia, S., I. A. Simpson, S. J. Vannucci, and A. Carruthers. The in vivo neuron-to-astrocyte lactate shuttle in human brain: evidence from modeling of measured lactate levels during visual stimulation. J. Neurochem. 109(Suppl 1):55-62, 2009.
42. Marangoni, A. G. Enzyme Kinetics, a Modern Approach. Hoboken: Wiley, 2003.
43. Mintun, M. A., A. G. Vlassenko, M. M. Rundle, and M. E. Raichle. Increased lactate/pyruvate ratio augments blood flow in physiologically activated human brain. Proc. Nat. Acad. Sci. U.S.A. 101:659-664, 2003.
44. Morris, A. A. M. Cerebral ketone body metabolism. J. Inherit. Metab. Dis. 28:109-121, 2005.
45. Occhipinti, R., M. A. Puchowicz, J. C. LaManna, E. Somersalo, and D. Calvetti. Statistical analysis of metabolic pathways of brain metabolism at steady state. Ann. Biomed. Eng. 6:886-902, 2007.
46. Occhipinti, R., E. Somersalo, and D. Calvetti. Interpretation of NMR spectroscopy human brain data with multicompartment computational model of cerebral metabolism. In: Oxygen Transport to Tissue XXXII, edited by J. C. LaManna, M. A. Puchowicz, K. Xu, D. K. Harrison, and D. F. Bruley, 2009, pp. 249-254.
47. Occhipinti, R., E. Somersalo, and D. Calvetti. Astrocytes as he glucose shunt for glutamatergic neurons at high activity: an in silico study. J. Neurophysiol. 101:2528-2538, 2009.
48. Occhipinti, R., E. Somersalo, and D. Calvetti. Energetics of inhibition: insights with a computational model of the human GABAergic neuron-astrocyte cellular complex. J. Cereb. Blood Flow Metab. 30:1834-1846, 2010.
49. Papin, J. A., J. Stelling, N. D. Price, S. Klamt, S. Shuster, and B. O. Palsson. Comparison of network-based pathway analysis methods. Trends Biotechnol. 22:400-405, 2004.
50. Pardo, B., T. B. Rodrigues, L. Contreras, M. Garzó n, I. Llorente-Folch, K. Kobayashi, T. Saheki, S. Cerdan, and J. Satrú stegui. Brain glutamine synthesis requires neuronal-born aspartate as amino donor for glial glutamate formation. J. Cereb. Blood Flow Metab. 31:90-101, 2011.
51. Pellerin, L., and P. J. Magistretti. Glutamate uptake into astrocytes stimulates aerobic glycolysis: a mechanism coupling neuronal activity to glucose utilization. Proc. Natl Acad. Sci. U.S.A. 91:10625-10629, 1994.
52. Pellerin, L., and P. J. Magistretti. Food for thought: challenging the dogmas. J. Cereb. Blood Flow Metab. 23:1282- 1286, 2003.
53. Schulman, R. G., F. Hyder, and D. L. Rothman. Lactate efflux and the neuroenergetic basis of brain function. NMR Biomed. 14:389-396, 2001.
54. Siesjö, B. K. Brain Energy Metabolism. New York: Wiley, 1978.
55. Simpson, I. A., A. Carruthers, and S. J. Vannucci. Supply and demand in cerebral energy metabolism: the role of nutrient transporters. J. Cereb. Blood Flow Metab. 27:1766-1791, 2007.
56. Vannucci, S. J., F. Maher, and I. A. Simpson. Glucose transporter proteins in brain: delivery of glucose to neurons and glia. Glia 21:2-21, 1997.
57. Zhou, L., J. E. Salem, G. E. Saidel, W. C. Stanley, and M. E. Cabrera. Mechanistic model of cardiac energy metabolism predicts localization of glycolysis to cytosolic subdomain during ischemia. Am. J. Physiol. Heart Circ. Physiol. 288:H2400-H2411, 2005.