Transportation in the Interstitial Space of the Brain Can Be Regulated by Neuronal Excitation

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Shi, Chunyan ^a,b   Lei, Yiming ^c   Han, Hongbin ^a,b   Zuo, Long ^a,b   Yan, Junhao ^b,d   He, Qingyuan ^a,b   Yuan, Lan ^d   Liu, Huipo ^e   Xu, Ge ^f   Xu, Weiguo ^g  

^a PEKING UNIVERSITY THIRD HOSPITAL   (China)

^b Key Lab of Magnetic Resonance Imaging Device and Technique   (China)

^c PEKING UNIVERSITY   (China)

^d PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

^e INSTITUTE OF APPLIED PHYSICS AND COMPUTATIONAL MATHEMATICS   (China)

^f UNIVERSITY OF SYDNEY   (Australia)

^g NATIONAL NATURAL SCIENCE FOUNDATION OF CHINA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GADOLINIUM PENTETATE;

ANIMAL; BRAIN; CAUDATE NUCLEUS; ELECTROSTIMULATION; EXTRACELLULAR FLUID; MALE; NERVE CELL; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PROCEDURES; SPRAGUE DAWLEY RAT; THALAMUS; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; BRAIN; CAUDATE NUCLEUS; ELECTRIC STIMULATION; EXTRACELLULAR FLUID; GADOLINIUM DTPA; MAGNETIC RESONANCE IMAGING; MALE; NEURONS; RATS, SPRAGUE-DAWLEY; THALAMUS;

EID: 84949256547     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17673     Document Type: Article

References (50)

1. Clasadonte, J., McIver, S. R., Schmitt, L. I., Halassa, M. M. & Haydon, P. G. Chronic sleep restriction disrupts sleep homeostasis and behavioral sensitivity to alcohol by reducing the extracellular accumulation of adenosine. J. Neurosci. 34, 1879-1891 (2014).
2. Xie, L. et al. Sleep drives metabolite clearance from the adult brain. Science 342, 373-377 (2013).
3. Tschumperlin, D. J. et al. Mechanotransduction through growth-factor shedding into the extracellular space. Nature 429, 83-86 (2004).
4. Kuchibhotla, K. V. et al. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 59, 214-225 (2008).
5. Tsurugizawa, T., Ciobanu, L. & Le Bihan, D. Water diffusion in brain cortex closely tracks underlying neuronal activity. Proc. Natl. Acad. Sci. USA 110, 11636-11641 (2013).
6. Hrabetova, S. & Nicholson, C. Biophysical Properties of Brain Extracellular Space Explored with Ion-Selective Microelectrodes, Integrative Optical Imaging and Related Techniques. In Electrochemical Methods for Neuroscience (ed. A. C. Michael & L. M. Borland) (Boca Raton (FL), 2007).
7. Han, H. et al. A novel MRI tracer-based method for measuring water diffusion in the extracellular space of the rat brain. IEEE J. Biomed. Health Inform 18, 978-983 (2014).
8. Ammann, D. & Anker, P. Neutral carrier sodium ion-selective microelectrode for extracellular studies. Neurosci. lett. 57, 267-271 (1985).
9. Kochian, L. V., Shaff, J. E., Kuhtreiber, W. M., Jaffe, L. F. & Lucas, W. J. Use of an extracellular, ion-selective, vibrating microelectrode system for the quantification of K +, H +, and Ca2 + fluxes in maize roots and maize suspension cells. Planta 188, 601-610 (1992).
10. Sykova, E. & Nicholson, C. Diffusion in brain extracellular space. Physiol. Rev. 88, 1277-1340 (2008).
11. Fedrowitz, M., Potschka, H., Richter, A. & Loscher, W. A microdialysis study of striatal dopamine release in the circling rat, a genetic animal model with spontaneous lateralized rotational behavior. Neuroscience 97, 69-77 (2000).
12. Kanno, M., Matsumoto, M., Togashi, H., Yoshioka, M. & Mano, Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J. Neurol. Sci. 217, 73-81 (2004).
13. Herrera-Marschitz, M., Arbuthnott, G. & Ungerstedt, U. The rotational model and microdialysis: Significance for dopamine signalling, clinical studies, and beyond. Prog. Neurobiol. 90, 176-189 (2010).
14. Thorne, R. G., Hrabetova, S. & Nicholson, C. Diffusion of epidermal growth factor in rat brain extracellular space measured by integrative optical imaging. J. Neurophysiol. 92, 3471-3481 (2004).
15. Wolak, D. J., Pizzo, M. E. & Thorne, R. G. Probing the extracellular diffusion of antibodies in brain using in vivo integrative optical imaging and ex vivo fluorescence imaging. J. Control Release 197, 78-86 (2015).
16. Caravan, P., Ellison, J. J., McMurry, T. J. & Lauffer, R. B. Gadolinium(III) chelates as MRI contrast agents: structure, dynamics, and applications. Chem. Rev. 99, 2293-2352 (1999).
17. Xu, F., Han, H., Zhang, H., Pi, J. & Fu, Y. Quantification of Gd-DTPA concentration in neuroimaging using T(1)3D MP-RAGE sequence at 3.0 T. Magn. Reson. Imaging 29, 827-834 (2011).
18. Li, K. et al. Real-time magnetic resonance imaging visualization and quantitative assessment of diffusion in the cerebral extracellular space of C6 glioma-bearing rats. Neurosci. Lett. 543, 84-89 (2013).
19. Siegel, A. & Sapru, H. Essential Neuroscience. 2nd edition, Sec. 3 (ed. Taylor, C.) Ch. 9, 149-151 (Lippincott Williams & Wilkins, 2009).
20. Yang, P. F., Chen, D. Y., Hu, J. W., Chen, J. H. & Yen, C. T. Functional tracing of medial nociceptive pathways using activitydependent manganese-enhanced MRI. Pain 152, 194-203 (2011).
21. Baliousis, M. The Brain and Behavior: An Introduction to Behavioral Neuroanatomy. 3rd edition. Psychol. Med. 41, 2233-2234 (2011).
22. Deco, G., Rolls, E. T., Albantakis, L. & Romo, R. Brain mechanisms for perceptual and reward-related decision-making. Prog. Neurobiol. 103, 194-213 (2013).
23. Kastellakis, G., Cai, D. J., Mednick, S. C., Silva, A. J. & Poirazi, P. Synaptic clustering within dendrites: An emerging theory of memory formation. Prog. Neurobiol. 126, 19-35 (2015).
24. Xue, Y. X. et al. Depletion of perineuronal nets in the amygdala to enhance the erasure of drug memories. J. Neurosci. 34, 6647-6658 (2014).
25. Guerin, C., Olivi, A., Weingart, J. D., Lawson, H. C. & Brem, H. Recent advances in brain tumor therapy: local intracerebral drug delivery by polymers. Invest. New Drugs 22, 27-37 (2004).
26. Gulati, K., Aw, M. S. & Losic, D. Nanoengineered drug-releasing Ti wires as an alternative for local delivery of chemotherapeutics in the brain. Int. J. Nanomed. 7, 2069-2076 (2012).
27. Han, H., Li, K., Yan, J., Zhu, K. & Fu, Y. An in vivo study with an MRI tracer method reveals the biophysical properties of interstitial fluid in the rat brain. Sci. China Life Sci. 55, 782-787 (2012).
28. Xu, F. et al. Greatly improved neuroprotective efficiency of citicoline by stereotactic delivery in treatment of ischemic injury. Drug Deliv. 18, 461-467 (2011).
29. Abbott, N. J. Evidence for bulk flow of brain interstitial fluid: significance for physiology and pathology. Neurochem. Int. 45, 545-552 (2004).
30. Aso, T. et al. An intrinsic diffusion response function for analyzing diffusion functional MRI time series. NeuroImage 47, 1487-1495 (2009).
31. Thompson, J. K., Peterson, M. R. & Freeman, R. D. Single-neuron activity and tissue oxygenation in the cerebral cortex. Science 299, 1070-1072 (2003).
32. Mayhew, J. E. Neuroscience. A measured look at neuronal oxygen consumption. Science 299, 1023-1024 (2003).
33. Aime, S., Botta, M., Fasano, M. & Terreno, E. Lanthanide(III) chelates for NMR biomedical applications. Chem. Soc. Rev. 27, 19-29 (1998).
34. Jin, B. J., Zhang, H., Binder, D. K. & Verkman, A. S. Aquaporin-4-dependent K( + ) and water transport modeled in brain extracellular space following neuroexcitation. J. Gen. Physiol. 141, 119-132 (2013).
35. Branzoli, F., Techawiboonwong, A., Kan, H., Webb, A. & Ronen, I. Functional diffusion-weighted magnetic resonance spectroscopy of the human primary visual cortex at 7 T. Magn. Reson. Med. 69, 303-309 (2013).
36. Parameshwaran, K., Dhanasekaran, M. & Suppiramaniam, V. Amyloid beta peptides and glutamatergic synaptic dysregulation. Exp. Neurol. 210, 7-13 (2008).
37. Suh, M., Choi-Kwon, S. & Kim, J. S. Sleep disturbances after cerebral infarction: role of depression and fatigue. J. Stroke Cerebrovasc. Dis. 23, 1949-1955 (2014).
38. Le Bihan, D. & Johansen-Berg, H. Diffusion MRI at 25: Exploring brain tissue structure and function. NeuroImage 61, 324-341 (2012).
39. Dietzel, I., Heinemann, U., Hofmeier, G. & Lux, H. D. Stimulus-induced changes in extracellular Na + and Cl- concentration in relation to changes in the size of the extracellular space. Exp. Brain Res. 46, 73-84 (1982).
40. Ransom, B. R., Yamate, C. L. & Connors, B. W. Activity-dependent shrinkage of extracellular space in rat optic nerve: a developmental study. J. Neurosci. 5, 532-535 (1985).
41. Nagelhus, E. A. & Ottersen, O. P. Physiological roles of aquaporin-4 in brain. Physiol. Rev. 93, 1543-1562 (2013).
42. Siegel, A. & Sapru, H. Essential Neuroscience. 2nd edition, Sec. 2 (ed. Taylor, C.) Ch. 5, 62-68 (Lippincott Williams & Wilkins, 2009).
43. Wolak, D. J. & Thorne, R. G. Diffusion of macromolecules in the brain: implications for drug delivery. Mol. Pharmaceut. 10, 1492-1504 (2013).
44. Dietzel, I., Heinemann, U., Hofmeier, G. & Lux, H. D. Transient changes in the size of the extracellular-space in the sensorimotor cortex of cats in relation to stimulus-induced changes in potassium concentration. Exp. Brain Res. 40, 432-439 (1980).
45. Vargova, L. & Sykova, E. Astrocytes and extracellular matrix in extrasynaptic volume transmission. Philos. T. R. Soc. B. 369 (2014).
46. Gonzalez-Flecha, B., Cutrin, J. C. & Boveris, A. Time course and mechanism of oxidative stress and tissue damage in rat liver subjected to in vivo ischemia-reperfusion. J. Clin. Invest. 91, 456-464 (1993).
47. Milanski, M. et al. Inhibition of hypothalamic inflammation reverses diet-induced insulin resistance in the liver. Diabetes 61, 1455-1462 (2012).
48. Liu, B., Bai, X. Z., Zhou, F. G., Han, H. B. & Hou, C. "Mutual information based three-dimensional registration of rat brain magnetic resonance imaging time-series". Comput. Electr. Eng. 39, 1473-1484 (2013).
49. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates, compact 6th edition, the Coronal Sections, figures 1-161 (Academic press, 2009).
50. Wang, J. Y., Luo, F., Chang, J. Y., Woodward, D. J. & Han, J. S. Parallel pain processing in freely moving rats revealed by distributed neuron recording. Brain Res. 992, 263-271 (2003).