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The Dendritic Cytoskeleton as a Computational Device: An Hypothesis

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Book cover The Emerging Physics of Consciousness

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Summary

This chapter presents a molecular-dynamical description of the functional role of cytoskeletal elements within the dendrites of a neuron. Our working hypothesis is that the dendritic cytoskeleton, including both microtubules (MTs) and actin filaments plays an active role in computations affecting neuronal function. These cytoskeletal elements are affected by, and in turn regulate, ion-channel activity, MAPs and other cytoskeletal proteins such as kinesin. A major hypothesis we advance here is that the C-termini protruding from the surface of a MT can exist in several conformational states, which lead to collective dynamical properties of the neuronal cytoskeleton. Further, these collective states of the C-termini on MTs have a significant effect on the ionic condensation and ion-cloud propagation that have physical similarities to those recently found in actin filaments. Our objective is to provide an integrated view of these phenomena in a bottom-up scheme. We outline substantial evidence to support our model and contend that ionic wave propagation along cytoskeletal structures impact channel function, and thus the computational capabilities of the dendritic tree and neuronal function at large.

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References

  1. Al-Bassam, J., R.S. Ozer, D. Safer, S. Halpain, and, R.A. Milligan. (2002). J. Cell Biol. 157:1187–1196.

    Article  Google Scholar 

  2. Alberts, B., A. Johnson, J. Lewis, M. Raff, K. Roberts, and, P. Walter. (2002). Molecular Biology of the Cell. Garland Science Publishing, New York.

    Google Scholar 

  3. Anderson, C.F. and Record, M.T. Jr. (1990). Ann. Rev. Biophys. Biophys. Chem. 19:423–465.

    Article  Google Scholar 

  4. Baverstock, K.F. and Cundall, R.B. (1988). Nature. 332:312–313.

    Article  ADS  Google Scholar 

  5. Beaumont, V., N. Zhong, R.C. Froemke, R.W. Ball, and, R.S. Zucker. (2002). Neuron. 33:601–613.

    Article  Google Scholar 

  6. Bernardo, L.S., L.M. Masukawa, and D. Prince. (1982). J. Neurosci. 2:1614–1622.

    Google Scholar 

  7. Bishop, C. (1995). Neural Networks for Pattern Recognition. Oxford University Press, Oxford.

    Google Scholar 

  8. Bliss, T.P. and G. Collingridge. (1993). Nature. 361:31–39.

    Article  ADS  Google Scholar 

  9. Caceres, A., M.R. Payne, L.I. Binder, and O. Steward. (1983). Proc Natl Acad Sci USA. 80:1738–1742.

    Article  ADS  Google Scholar 

  10. Cantiello, H.F., C.R. Patenaude, and K.S. Zaner. (1991). Biophys. J. 59:1284–1289.

    Article  ADS  Google Scholar 

  11. Challacombe, J.F., D.M. Snow, and P.C. Letourneau. (1996). J. Cell Sci. 109:2031–2040.

    Google Scholar 

  12. Challacombe, J.F., D.M. Snow, and P.C. Letourneau. (1997). J. Neurosci. 17:3085–3095.

    Google Scholar 

  13. Chasan, B., N.A. Geisse, K. Pedatella, D.G. Wooster, M. Teintze, M.D. Carattino, W.H. Goldmann, and H.F. Cantiello. (2002). Eur. Biophys. J. 30:617–624.

    Article  Google Scholar 

  14. Christie, B.R., D.S. Kerr, and W. Abraham. (1994). Hippocampus. 4.

    Google Scholar 

  15. Colicos, M.A., B.E. Collins, M.J. Sailor, and Y. Goda. (2001). Cell. 30:605–616.

    Article  Google Scholar 

  16. Coppin, C. and P. Leavis. (1992). Biophys J. 63:794–807.

    Article  Google Scholar 

  17. Correas, I., R. Padilla, and J. Avila. (1990). Biochem. J. 269:61–64.

    Google Scholar 

  18. Crick, F. (1982). Trends Neurosci. 5:44–46.

    Article  Google Scholar 

  19. Davydov. (1982). In International Series in Natural Phylosophy. D. Haav, (ed.) Pergamon, Oxford, UK.

    Google Scholar 

  20. de Schutter, E. (1998). J. Neurophysiol. 80:504–519.

    Google Scholar 

  21. Dehmelt, L. and S. Halpain. (2004). J. Neurobiol. 58:18–33.

    Article  Google Scholar 

  22. Dehmelt, L., F.M. Smart, R.S. Ozer, and S. Halpain. (2003). J. Neurosci. 23:9479–9490.

    Google Scholar 

  23. Dent, E.W. and K. Kalil. (2001). J. Neurosci. 21:9757–9769.

    Google Scholar 

  24. Dunaevsky, A., A. Tashiro, A. Majewska, C. Mason, and R. Yuste. (1999). Proc. Natl. Acad. Sci. USA. 96:13438–13443.

    Article  ADS  Google Scholar 

  25. Dustin, P. (1984). Microtubules. Springer-Verlag, Berlin.

    Google Scholar 

  26. Edson, K., B. Weisshaar, and A. Matus. (1993). Development. 117:689–700.

    Google Scholar 

  27. Engert, F. and T. Bonhoeffer. (1999). Nature. 399:66–70.

    Article  ADS  Google Scholar 

  28. Fifkova, E. and R.J. Delay. (1982). J. Cell Biol. 95:345–350.

    Article  Google Scholar 

  29. Fischer, M., S. Kaech, D. Knutti, and A. Matus. (1998). Neuron. 20:847–854.

    Article  Google Scholar 

  30. Fischer, M., S. Kaech, U. Wagner, H. Brinkhaus, and A. Matus. (2000). Nature Neurosci. 3:887–894.

    Article  Google Scholar 

  31. Forscher, P. and S.J. Smith. (1988). J. Cell Biol. 107:1505–1516.

    Article  Google Scholar 

  32. Fukazawa, Y., Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi. (2003). Neuron. 38:447–460.

    Article  Google Scholar 

  33. Furukawa, R., R. Kundra, and M. Fechheimer. (1993). Biochem. 32:12346–12352.

    Article  Google Scholar 

  34. Garrido, J.J., F. Fernandes, A. Moussif, M.-P. Fache, P. Giraud, and B. Dargent. (2003). Biology of the Cell. 95:437–445.

    Article  Google Scholar 

  35. Greenough, W. (1975). Am. Sci. 63:37–46.

    ADS  Google Scholar 

  36. Griffith, L.M. and T.D. Pollard. (1982). J. Biol. Chem. 257:9143–9151.

    Google Scholar 

  37. Hebb, D.O. (1949). The Organization of Behavior: A Neuropsychological Theory. John Wiley, New York.

    Google Scholar 

  38. Hempel, C.M., K.H. Hartman, X.J. Wang, G.G. Turrigiano, and S.B. Nelson. (2000). J. Neurophysiol. 83:3031–3041.

    Google Scholar 

  39. Hering, H. and M. Sheng. (2001). Nat. Rev. Neurosci. 2:880–888.

    Article  Google Scholar 

  40. Hille, B. (1992). Ionic Channels of Excitable Membranes. Sinauer Associates Inc., Sunderland, MA.

    Google Scholar 

  41. Hodgkin, A.L. and A.F. Huxley. (1952). J. Physiol. 117:500–544.

    Google Scholar 

  42. Holmes, K.C., D. Popp, W. Gebhard, and W. Kabsch. (1990). Nature. 347:44–49.

    Article  ADS  Google Scholar 

  43. Jaffe, D.B., D. Johnston, N. Lasser-Ross, E. Lisman, H. Miyakawa, and W. Ross. (1992). Nature. 357:244–246.

    Article  ADS  Google Scholar 

  44. Jaffe, D.B., W.N. Ross, J.E. Lisman, N. Lasser-Ross, H. Miyakawa, and D. Johnston. (1994). J. Neurophysiol. 71:1065–1077.

    Google Scholar 

  45. Janmey, P. (1998). Physiol. Rev. 78:763–781.

    Google Scholar 

  46. Jaslove, S. (1992). Neurosci. 47:495–495I499.

    Article  Google Scholar 

  47. Johnson, B.D. and L. Byerly. (1993). Neuron:797–804.

    Google Scholar 

  48. Johnson, B.D. and L. Byerly. (1994). Pflügers Arch. 429:14–21.

    Article  Google Scholar 

  49. Johnston, D., J.C. Magee, C.M. Colbert, and B.R. Christie. (1996). Annu. Rev. Neurosci. 19:165–186.

    Article  Google Scholar 

  50. Johnston, D., S. Williams, D. Jaffe, and R. Gray. (1992). Annu. Rev. Physiol. 54:489–505.

    Article  Google Scholar 

  51. Kabsch, W., H.G. Mannherz, D. Suck, E.F. Pai, and K.C. Holmes. (1990). Nature. 347:37–44.

    Article  ADS  Google Scholar 

  52. Kaech, S., H. Brinkhaus, and A. Matus. (1999). Proc. Natl. Acad. Sci. USA. 96:10433–10437.

    Article  ADS  Google Scholar 

  53. Kaech, S., H. Parmar, M. Roelandse, C. Bornmann, and A. Matus. (2001). Proc. Natl. Acad. Sci. USA. 98:7086–7092.

    Article  ADS  Google Scholar 

  54. Khuchua, Z., D.F. Wozniak, M.E. Bardgett, Z. Yue, M. McDonald, J. Boero, R.E. Hartman, H. Sims, and A.W. Strauss. (2003). Neurosci. 119:101–111.

    Article  Google Scholar 

  55. Kiebler, M.A. and L. DesGroseillers. (2000). Neuron. 25:19–28.

    Article  Google Scholar 

  56. Kim, C.-H. and J.E. Lisman. (1999). J. Neurosci. 19:4314–4324.

    Google Scholar 

  57. Knowles, R., N. LeClerc, and K.S. Kosik. (1994). Cell Motil. Cytoskeleton. 28:256–264.

    Article  Google Scholar 

  58. Kobayasi, S. (1964). Biochim. Biophys. Acta. 88:541–552.

    Google Scholar 

  59. Kobayasi, S., H. Asai, and F. Oosawa. (1964). Biochim. Biophys. Acta. 88:528–540.

    Google Scholar 

  60. Koch, C. and I. Segev. (2000). Nature Neurosci. 3:1171–1177.

    Article  Google Scholar 

  61. Kolosick, J.A., D.L. Landt, H.C. S. Hsuan, and K.E. Lonngren. (1974). Proc. IEEE. 62:578–581.

    Article  Google Scholar 

  62. Lader, A.S., H.N. Woodward, E.C. Lin, and H.F. Cantiello. (2000). In MEMTMBS. Faramaz, V., (ed.) CRA, Las Vegas, NV. 77–82.

    Google Scholar 

  63. Landis, D.M. and T.S. Reese. (1983). J. Cell Biol. 97:1169–1178.

    Article  Google Scholar 

  64. Lee, T., S. Marticke, C. Sung, S. Robinow, and L. Luo. (2000). Neuron. 28:807–818.

    Article  Google Scholar 

  65. Lester, R.J., J.D. Clements, G.L. Westbrook, and C. Jahr. (1990). Nature. 346:565–567.

    Article  ADS  Google Scholar 

  66. Letourneau, P.C. (1996). Perspect Dev. Neurobiol. 4:111–123.

    Google Scholar 

  67. Letourneau, P.C. and A.H. Ressler. (1984). J. Cell Biol. 98:1355–1362.

    Article  Google Scholar 

  68. Liao, G., T. Nagasaki, and G.G. Gundersen. (1995). J. Cell Sci. 108:3473–3483.

    Google Scholar 

  69. Lin, C.H., C.A. Thompson, and P. Forscher. (1994). Curr. Opin. Neurobiol. 4:640–647.

    Article  Google Scholar 

  70. Lin, E. and H.F. Cantiello. (1993). Biophys. J. 65:1371–1378.

    Article  Google Scholar 

  71. Lonngren, K.E. (1978). In Solitons in Action. K.E. Lonngren and A. Scott (eds.) Academic Press, New York. 127–152.

    Google Scholar 

  72. Lonngren, K.E., D.L. Landt, C.M. Burde, and J.A. Kolosick. (1975). IEEE Trans. Circuits and Systems. CAS-22:376–378.

    Article  Google Scholar 

  73. Luo, L. (2002). Annu. Rev. Cell Develop. Biol. 18:601–635.

    Article  Google Scholar 

  74. Maguire, G., Connaughton, V., Prat, A.G., Jackson Jr., G.R. and H.F. Cantiello. (1998). NeuroReport. 9:665–670.

    Article  Google Scholar 

  75. Malenka, R. (1991). Mol. Neurobiol. 5:289–295.

    Article  Google Scholar 

  76. Manning, G.S. (1969). J. Chem. Phys. 51:924–933.

    Article  ADS  Google Scholar 

  77. Manning, G.S. (1978). Quarterly Rev. Biophys. 2:179–246.

    Article  Google Scholar 

  78. Matus, A. (2000). Science. 290:754–758.

    Article  ADS  Google Scholar 

  79. Matus, A., M. Ackermann, G. Pehling, H.R. Byers, and K. Fujiwara. (1982). Proc. Natl. Acad. Sci. USA. 79:7590–7594.

    Article  ADS  Google Scholar 

  80. McCullogh, W.S. and W. Pitts. (1943). Bull. Math. Biophys. 5:115–133.

    Article  MathSciNet  Google Scholar 

  81. Mel, B.W. (1999). In Dendrites. G. Stuart, N. Spruston, and M. Hausser (eds.) Oxford University Press, Oxford.

    Google Scholar 

  82. Meunier, C., I. Segev, and D. Zytnicki. (1999). J. Physiol. (Paris). 93:261.

    Article  Google Scholar 

  83. Miyakawa, H., W.N. Ross, D. Jaffe, J.C. Callaway, N. Laser-Ross, et al. (1992). Neuron. 9:1163–1173.

    Article  Google Scholar 

  84. Morales, M. and E. Fifkova. (1989). Cell Tissue Res. 256:447–456.

    Article  Google Scholar 

  85. Natschlger, T., W. Maass, and H. Makram. (2002). Foundations of Information Processing of TELEMATIK (special issue). 8:39–42.

    Google Scholar 

  86. Noguchi, A. (1974). Elec. and Comm. in Japan. 57-A:9–13.

    ADS  Google Scholar 

  87. Noiges, R., R. Eichinger, W. Kutschera, I. Fischer, Z. Nemeth, G. Wiche, and F. Propst. (2002). J. Neurosci. 22:2106–2114.

    Google Scholar 

  88. O’Leary, D.D.M. and S.E. Koester. (1993). Neuron. 10:991–1006.

    Article  Google Scholar 

  89. Oosawa, F. (1970). Biopolymers. 9:677–688.

    Article  Google Scholar 

  90. Oosawa, F. (1971). Polyelectrolytes. Marcel Dekker, Inc., New York.

    Google Scholar 

  91. Ostrovskii, L.A., V.V. Papko, and E.N. Pelinovskii. (1974). Radiophysics and Quantum Electronics. 15:438–446.

    Article  ADS  Google Scholar 

  92. Ozer, R.S. and S. Halpain. (2000). Mol. Biol. Cell. 11:3573–3587.

    Google Scholar 

  93. Parodi, M., B. Bianco, and A. Chiabrera. (1985). Cell Biophys. 7:215–235.

    Google Scholar 

  94. Passafaro, M., C. Sala, M. Niethammer, and M. Sheng. (1999). Nature Neurosci. 2:1063–1069.

    Article  Google Scholar 

  95. Pedrotti, B., R. Colombo, and K. Islam. (1994). Biochemistry. 33:8798–8806.

    Article  Google Scholar 

  96. Pedrotti, B. and K. Islam. (1996). FEBS Lett. 388:131–133.

    Article  Google Scholar 

  97. Pollard, T.D. and J.A. Cooper. (1986). Ann. Rev. Biochem. 55:987–1035.

    Article  Google Scholar 

  98. Tuszynski J.A., Priel, A. and Woolf, N. (2004). Submitted to European Biophysics Journal.

    Google Scholar 

  99. Rall, W. (1959). Exp. Neurol. 1:491–527.

    Article  Google Scholar 

  100. Rall, W. and J. Rinzel. (1973). Biophys. J. 13:648–688.

    Article  ADS  Google Scholar 

  101. Ramon-Moliner, E. (1968). In The Structure and Function of Nervous Tissue. G.H. Bourne (ed.) Academic Press, New York. 205–267.

    Google Scholar 

  102. Regehr, W.G., J.A. Connor, and D. Tank. (1989). Nature. 341:533–536.

    Article  ADS  Google Scholar 

  103. Regehr, W.G. and D. Tank. (1990). Nature. 345:807–810.

    Article  ADS  Google Scholar 

  104. Regehr, W.G. and D. Tank. (1992). J. Neurosci. 12:4202–4223.

    Google Scholar 

  105. Rihn, L.L. and B. Claiborne. (1990). Dev. Brain Res. 54:115–124.

    Article  Google Scholar 

  106. Rochlin, M.W., K.M. Wickline, and P.C. Bridgman. (1996). J. Neurosci. 16:3236–3246.

    Google Scholar 

  107. Rodriguez, O.C., A.W. Schaefer, C.A. Mandato, P. Forscher, W.M. Bement, and C.M. Waterman-Storer. (2003). Nature Cell Biol. 5:599–609.

    Article  Google Scholar 

  108. Sackett, D.L. (1995). In Subcellular Biochemistry-Proteins: Structure, function and engineering. B. Biswas, B. and Roy, S. (eds.) Kluwer Academic Publishers, Dordrecht. 255–302.

    Google Scholar 

  109. Salmon, W.C., M.C. Adams, and C.M. Waterman-Storer. (2002). J. Cell Biol. 158:31–37.

    Article  Google Scholar 

  110. Sanes, J.R. and J.W. Lichtman. (1999). Annu. Rev. Neurosci. 22:389–342.

    Article  Google Scholar 

  111. Sarmiere, P.D. and J.R. Bamburg. (2004). J. Neurobiol. 58:103–117.

    Article  Google Scholar 

  112. Sataric, M.V., J.A. Tuszynski, and R.B. Zakula. (1993). Phys. Rev. E. 48:589–597.

    Article  ADS  Google Scholar 

  113. Sattilaro, W. (1986). Biochemistry. 25:2003–2009.

    Article  Google Scholar 

  114. Schaefer, A.W., N. Kabir, and P. Forscher. (2002). J. Cell Biol. 158:139–152.

    Article  Google Scholar 

  115. Schiller, J., G. Major, H.J. Koester, and Y. Schiller. (2000). Nature. 404:185–289.

    Article  Google Scholar 

  116. Schwartzkroin, P.A. and M. Slawsky. (1977). Brain Res. 135:157–161.

    Article  Google Scholar 

  117. Scott, E.K. and L. Luo. (2001). Nat. Neurosci. 4:359–365.

    Article  Google Scholar 

  118. Segel, L. and H. Parnas. (1991). In Biologically Inspired Physics. Peliti, L. (ed.) Plenum Press, New York.

    Google Scholar 

  119. Segev, I. and M. London. (2000). Science. 290:744–750.

    Article  ADS  Google Scholar 

  120. Selden, S.C. and T. Pollard. (1983). J. Biol. Chem. 258:7064–7071.

    Google Scholar 

  121. Sept, D., J. Xu, T. Pollard, and J. McCammon. (1999). Biophys. J. 77:2911–2919.

    Article  Google Scholar 

  122. Shepherd, G.M., R.K. Brayton, M.J.P., I. Segev, J. Rinzel, and W. Rall. (1985). Proc. Natl. Acad. Sci. USA. 82:2192–2195.

    Article  ADS  Google Scholar 

  123. Smith, C.L. (1994). J. Cell Biol. 127:1407–1418.

    Article  Google Scholar 

  124. Softky, W. (1994). Neurosci. 58:13–41.

    Article  Google Scholar 

  125. Spruston, N., D.B. Jaffe, and D. Johnston. (1994). Trends Neurosci. 17:161–166.

    Article  Google Scholar 

  126. Steward, O. and E.M. Schuman. (2001). Annu. Rev. Neurosci. 24:299–325.

    Article  Google Scholar 

  127. Tanaka, E.M. and M.W. Kirschner. (1991). J. Cell Biol. 115:345–363.

    Article  Google Scholar 

  128. Tang, J.X. and P.A. Janmey. (1996). J. Biol. Chem. 271:8556–8563.

    Article  Google Scholar 

  129. Technau, G. and M. Heisenberg. (1982). Nature. 295:405–407.

    Article  ADS  Google Scholar 

  130. Thorn, K.S., J.A. Ubersax, and R.D. Vale. (2000). J. Cell Biol. 151:1093–1100.

    Article  Google Scholar 

  131. Togel, M., G. Wiche, and F. Propst. (1998). J. Cell Biol. 143:695–707.

    Article  Google Scholar 

  132. Toni, N., P.A. Buchs, I. Nikonenko, C.R. Bron, and D. Muller. (1999). Nature. 402:421–425.

    Article  ADS  Google Scholar 

  133. Truman, J.W. and S.E. Reiss. (1976). Science. 192:477–479.

    Article  ADS  Google Scholar 

  134. Tuszynski, J.A., S. Portet, J.M. Dixon, C. Luxford, and H.F. Cantiello. (2004). Biophys. J. 86:1890–1903.

    Article  ADS  Google Scholar 

  135. Varela, J.A., K. Sen, J. Gibson, J. Fost, L.F. Abbott, and S.B. Nelson. (1997). J. Neurosci. 17:7926–7940.

    Google Scholar 

  136. Wang, Y.L. (1985). J. Cell Biol. 101:597–602.

    Article  Google Scholar 

  137. Wang, Z. and M.P. Sheetz. (2000). Biophys. J. 78:1955–1964.

    Article  Google Scholar 

  138. Weimann, J.M., A. Zhang, M.E. Levin, W.P. Devine, P. Brulet, and S.K. Mc-Connell. (1999). Neuron. 24:819–831.

    Article  Google Scholar 

  139. Wong, R.W., M. Setou, J. Teng, Y. Takei, and N. Hirokawa. (2002). Proc. Natl. Acad. Sci. USA. 99:14500–14505.

    Article  ADS  Google Scholar 

  140. Woolf, N.J., M.D. Zinnerman, and G.V.W. Johnson. (1999). Brain Res. 821:241–249.

    Article  Google Scholar 

  141. Yuste, R. and T. Bonhoeffer. (2001). Annu. Rev. Neurosci. 24:1071–1089.

    Article  Google Scholar 

  142. Yuste, R., M.J. Gutnick, D. Saar, K.R. Delaney, and D. Tank. (1994). Neuron. 13:23–43.

    Article  Google Scholar 

  143. Yvon, A.M., P. Wadsworth, and M.A. Jordan. (1999). Mol. Biol. Cell. 10:947–959.

    Google Scholar 

  144. Zhang, W. and D.L. Benson. (2001). J. Neurosci. 15:5169–5181.

    Google Scholar 

  145. Zimm, B.H. (1986). In Coulombic Interactions in Macromolecular Systems. Eisenberg, A. and Bailey, F.E. (eds.) American Chemical Society, Washington D.C.:212–215.

    Chapter  Google Scholar 

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Priel, A., Tuszynski, J.A., Cantiello, H.F. (2006). The Dendritic Cytoskeleton as a Computational Device: An Hypothesis. In: Tuszynski, J.A. (eds) The Emerging Physics of Consciousness. The Frontiers Collection. Springer, Berlin, Heidelberg. https://doi.org/10.1007/3-540-36723-3_8

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