Modulation of CNS excitability by water movement. the D2O effects on the non-linear neuron-glial dynamics

DOI: 10.4236/jbpc.2011.23040   PDF   HTML   XML   5,288 Downloads   8,332 Views   Citations


Macroscopic spatiotemporal patterns arising in grey matter may explain the clinical manifestations of several functional neurological syndromes (migraine aura, epilepsies). Detailed descriptions of these patterns in central grey matter and their physicochemical or pharmacological manipulations can be useful in many scientific fields ranging from drug design to functional brain imaging. These evanescent dynamic structures are electrochemical in nature and show macroscopic tissue polarization due to coupled and macroscopic flow of ions and water across, along and between neuronal and glial membranes. So far the importance of the water flow in the CNS functional syndromes has been examined by manipulations of water channels aquaporines (AQP). In this paper we show the result of substituting H2O for D2O in retinal spreading depression experiments. This inverts the present logic by changing the flow in the water channels in intact tissue and observing the evolution of electrochemical patterns and recording the optical profiles of excitation waves in isolated chick retinas. D2O flow through AQPs is ~20% slower than that of H2O. The slower flux disturbs the tight coupling between ion and water flows across membranes and slowdown the Na-KATPase rate of change with metabolic consequences for the tissue. The whole tissue excitability shifts in a non-stationary manner toward a non-excitable state.

Share and Cite:

Lima, V. and Hanke, W. (2011) Modulation of CNS excitability by water movement. the D2O effects on the non-linear neuron-glial dynamics. Journal of Biophysical Chemistry, 2, 353-360. doi: 10.4236/jbpc.2011.23040.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Dowling, J. (1987) The retina, an approachable part of the brain. Harvard University Press, Cambridge.
[2] Gouras, P. (1958) Spreading depression of activity in amphibian retina. American Journal of Physiology, 195, 28-32.
[3] Martins-Ferreira, H., De Castro, G.O. (1966) Light scattering changes accompanying spreading depression in isolated chicken retina. Journal of Neurophysiology, 29, 715-726.
[4] De Castro, G.O., Martins-Ferreira, H. and Gardino, P.F. (1985) Dual nature of the peaks of light scattered during spreading depression in chick retina. Anais da Academia Brasileira de Ciências, 57, 95-103.
[5] Do Carmo, R. and Martins-Ferreira, H. (1984) Spreading depression of Le?o probed with ion-sensitive electrodes Anais da Academia Brasileira de Ciências, 56, 401-421.
[6] Fernandes de Lima, V.M. and Hanke, W. (1997) Excitation waves in central gray matter: The retinal spreading depression. Progress in Retinal and Eye Research, 6, 657-690.
[7] Peixoto, N.L.V., Fernandes de Lima, V.M. and Hanke, W. (2001) Correlation of the electrical and intrinsic optical signals in the chicken spreading depression phenomenon. Neuroscience Letters, 299, 89-92.
[8] Wiedemann, M., De Lima, V.M.F. and Hanke, W. (2001) Gravity dependence of waves in the retinal spreading depression and in gel type Belouov-Zabothinsky systems. Physical Chemistry Chemical Physics, 4, 1370-1373. doi:10.1039/b109166m
[9] Weimer, M.S. and Hanke, W. (2005) Correlation between the durations of refractory period and intrinsic optical signal of spreading depression during temperature variations. Experimental Brain Research, 161, 201-208. doi:10.1007/s00221-004-2060-5
[10] Katchalsky, A. (1971) Carriers and specificity in membranes. VI Biological flow structure and their relation to chemodiffusion coupling. Neurosciences Research Program Bulletin, 9, 397-413.
[11] Katchalsky, A. (1975) Concept of dynamic patterns. Neurosciences Research Program Bulletin, 12, 11-26, 30-52.
[12] Katchalsky, A. (1971) Polyelectrolytes and their biological interactions. Biophysical Journal, 4, 9-41.
[13] Tait, M.J., Saadoun, S., Bell, A. and Papadopulos, M.C. (2007) Water movement in the brain: Role of aquaporins. TRENDS in Neurosciences, 31, 27-43.
[14] Binder, D. and Steinhauser, C. (2006) Functional changes in astroglial cells in epilepsy. Glia, 54, 358-368. doi:10.1002/glia.20394
[15] Panicke, T., Iandiev, I., Uckermann, O., Biedermann, B., Kutzera, F., Wiedemann, P., Wolburg, H., Reichenbach, A. and Bringmann, A. (2004) A potassium channel linked mechanism of glial cell swelling in the postischemic retina. Molecular and Cellular Neuroscience, 26, 493-502. doi:10.1016/j.mcn.2004.04.005
[16] Goodyear, M.J., Crewther, S.G., Murphy, M., Giumarra, L., Hazi, A., Junghans, B.M. and Crewthers, D. (2010) Spatial and temporal dissociation of AQP4 and Kir4.1 expression during induction of refractive errors. Molecular Vision, 16, 1610-1619.
[17] Mamonov, A.B., Coalson, R.D., Zeidel, M.L. and Mathai, J.C. (2007) Water and deuterium oxide permeability through aquaporin-1: MD predictions and experimental verification. The Journal of General Physiology, 130, 111-116. doi:10.1085/jgp.200709810
[18] Pittendrigh, C.S., Caldarola, P.C. and Cosbey, E.S. (1973) A differential effect of heavy water on temperature dependent and temperature compensated aspects of the circadian system of the drosophila pseudoobscura. Proceedings of the National Academy of Sciences of the United States of America, 70, 2037-2041. doi:10.1073/pnas.70.7.2037
[19] MacDaniel, M., Sulzman, F.M. and Hastings, J.W. (1974) Heavy water slows the Goniaulax clock: A test of the hipothesys that D2O affects circadian oscillations by diminishing the apparent temperature. Proceedings of the National Academy Sciences of the United States of America, 71, 4389-4391. doi:10.1073/pnas.71.11.4389
[20] Landowner, D. (1987) D2O and the sodium pump in squid nerve membrane. Journal of Membrane Biology, 96, 277-281. doi:10.1007/BF01869309
[21] Fernandes de Lima, V.M., Weimer, M. and Hanke, W. (2002) Spectral dependence of the intrinsic optical signal of excited states of central gray matter and conformational changes at membrane interfaces. Physical Chemistry Chemical Physics, 4, 1374-1379. doi:10.1039/b109914k
[22] Whittam, R. (1962) The dependence of respiration of brain cortex on active ion transport. Biochemical Journal, 82, 205-212.
[23] Whittam, R. and Blond, D.M. (1964) Respiratory control by an adenosine triphosphatase involved in active transport in brain cortex. Biochemical Journal, 92, 147-158.
[24] Dahlem, Y.A. and Hanke, W. (2005) Intrinsic optical signal of spreading depression: Second phase depends on energy metabolism and nitric oxide. Brain Research, 1049, 15-24. doi:10.1016/j.brainres.2005.04.059
[25] Klink, O., Hanke, W., Gebershagen, E. and Fernandes de Lima, V.M. (2010) Influence of heavy water on waves and oscillations in the Belouzov-Zabotinsky reaction. In: Petrin, A., Ed., Wave Propagation in Materials for Modern Applications, InTech Books, Morn Hill, 21.
[26] Dahlem, M. and Hadjikahani, N. (2009) Migraine aura: Retracting particle-like waves in weakly susceptible cortex. PLoS ONE, 4, e5007. doi:10.1371/journal.pone.0005007
[27] Streit, D.S. (1990) Depress?o alastrante retiniana in vivo (1990) MSc Thesis presented to the Ophtalmology Department UFRJ, Rio de Janeiro, Brazil.
[28] Ferreira Filho, C.R. and Martins-Ferreira, H. (1992) Interstitial fluid pH and its change during spreading depression in isolated chicken retina. In: DoCarmo, R., Ed., Spreading Depression, Springer Verlag, Berlin, 75-88.
[29] Xu, J.-Y., Huang, X. and Zhang, C. (2008) Propagating waves of activity in the neocortex: What they are, what they do. Neuroscientist, 14, 487-502.
[30] Hermann, G.E., Van Meter, M.J., Roo, J.C. and Rogers, R.C. (2009) Proteinase activated receptors in the nucleus of the solitary tract: evidence for glial-neural interactions in autonomic control of the stomach. The Journal of neuroscience, 29, 9292-9300.
[31] Lee, C.J., Mannaioni, G., Yuan, H., Woo, D.H., Gingrich, M.B. and Traynelis, S.F. (2007) Astrocytic control of synaptic NMDA receptors. The Journal of Physiology, 581, 1057-1081. doi:10.1113/jphysiol.2007.130377
[32] Fernandes de Lima, V.M. and Hanke, W. (1996) Observa- tions of non-stationatities in extracellualr potassium dy- namics within the gray matter neuropil during self-sus- tained SDs. Journal of Brain Research, 37, 505-518.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.