Skip to main content Accessibility help
×
Hostname: page-component-84b7d79bbc-rnpqb Total loading time: 0 Render date: 2024-07-31T01:29:12.762Z Has data issue: false hasContentIssue false

19 - Neuromechanobiology of the brain

Mechanics of neuronal structure, function, and pathophysiology

from Part II - Recent progress in cell mechanobiology

Published online by Cambridge University Press:  05 November 2015

Yu Sun
Affiliation:
University of Toronto
Deok-Ho Kim
Affiliation:
University of Washington
Craig A. Simmons
Affiliation:
University of Toronto
Get access

Summary

This chapter discusses recent progress and future directions regarding mechanobiology as applied to neuronal function. Along with the generation and transduction of mechanical forces by neuronal elements, the influence of mechanical forces on the neuronal membrane, actin, and ion channels is highlighted. Further topics such as cortical folding and traumatic brain injury expand discussion of the role of mechanical forces into a more macroscopic scale. As the mechanical properties of the nervous tissue environment and other mechanical cues influence neural development and contribute to the regulation of endogenous brain function, there is great utility in investigating the mechanical properties of the central nervous system. Through discussion of the role of mechanical forces in neural elements, and early biophysical formulations to understand neural systems that incorporate mechanical analysis, this chapter hopes to encourage expansion of studies and methods investigating mechanobiology applied to the nervous system.

Type
Chapter
Information
Integrative Mechanobiology
Micro- and Nano- Techniques in Cell Mechanobiology
, pp. 347 - 367
Publisher: Cambridge University Press
Print publication year: 2015

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, B. C., Hill, A. V., and Howarth, J. V.. (1958). “The positive and negative heat production associated with a nerve impulse.” Proc R Soc Lond B Biol Sci 148(931): 149187.Google ScholarPubMed
Ahmed, W. W., et al. (2012). “Mechanical tension modulates local and global vesicle dynamics in neurons.” Cell Mol Bioeng 5(2): 155164.CrossRefGoogle ScholarPubMed
Almeida, P. F. F. and Vaz, W. L. C.. (1995). “Lateral diffusion in membranes.” In Handbook of Biological Physics: Structure and Dynamics of Membranes – From Cells to Vesicles, Lipowsky, R. and Sackmann, E., eds. Amsterdam: North-Holland, 305357.CrossRefGoogle Scholar
Anava, S., et al. (2009). “The regulative role of neurite mechanical tension in network development.” Biophys J 96(4): 16611670.CrossRefGoogle ScholarPubMed
Arnadottir, J. and Chalfie, M.. (2010). “Eukaryotic mechanosensitive channels.” Annu Rev Biophys 39: 111137.CrossRefGoogle ScholarPubMed
Balice-Gordon, R.J. and Lichtman, J.W.. (1990). “In vivo visualization of the growth of pre– and postsynaptic elements of neuromuscular junctions in the mouse.” J Neurosci 10(3): 894908.CrossRefGoogle ScholarPubMed
Betz, T., et al. (2011). “Growth cones as soft and weak force generators.” Proc Natl Acad Sci USA 108(33): 1342013425.CrossRefGoogle ScholarPubMed
Bray, D. (1984). “Axonal growth in response to experimentally applied mechanical tension.” Dev Biol 102(2): 379–89.CrossRefGoogle ScholarPubMed
Bridgman, P. C., et al. (2001). “Myosin IIB is required for growth cone motility.” Journal of Neuroscience 21(16): 61596169.CrossRefGoogle ScholarPubMed
Cantor, R. S. (1997). “The lateral pressure profile in membranes: a physical mechanism of general anesthesia.” Biochemistry 36(9): 23392344.CrossRefGoogle ScholarPubMed
Chan, C. E. and Odde, D. J.. (2008). “Traction dynamics of filopodia on compliant substrates.” Science 322(5908): 16871691.CrossRefGoogle ScholarPubMed
Chen, B. M. and Grinnell, A. D.. (1995). “Integrins and modulation of transmitter release from motor nerve terminals by stretch.” Science 269(5230): 15781580.CrossRefGoogle ScholarPubMed
Cole, K. S. (1941). “Rectification and inductance in the squid giant axon.” J Gen Physiol 25(1): 2951.CrossRefGoogle ScholarPubMed
Crawford, G. E. and Earnshaw, J. C.. (1987). “Viscoelastic relaxation of bilayer lipid membranes. Frequency-dependent tension and membrane viscosity.” Biophys J 52(1): 8794.CrossRefGoogle ScholarPubMed
Elkin, B. S., et al. (2007). “Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation.” J Neurotrauma 24(5): 812–22.CrossRefGoogle ScholarPubMed
Evans, E.A. and Hochmuth, R.M., Current Topics in Membranes and Transport. 1978. 164.CrossRefGoogle Scholar
Eyckmans, J., et al. (2011). “A hitchhiker’s guide to mechanobiology.” Dev Cell 21(1): 3547.CrossRefGoogle ScholarPubMed
Farkas, O., Lifshitz, J., and Povlishock, J.T.. (2006). “Mechanoporation induced by diffuse traumatic brain injury: an irreversible or reversible response to injury?J Neurosci 26(12): 31303140.CrossRefGoogle ScholarPubMed
Farkas, O. and Povlishock, J. T.. (2007). “Cellular and subcellular change evoked by diffuse traumatic brain injury: a complex web of change extending far beyond focal damage.” Prog Brain Res 161: 4359.CrossRefGoogle ScholarPubMed
Fass, J. N. and Odde, D. J.. (2003). “Tensile force-dependent neurite elicitation via anti-beta 1 integrin antibody-coated magnetic beads.” Biophysical Journal 85(1): 623636.CrossRefGoogle Scholar
Fatt, P. and Katz, B.. (1952). “Spontaneous subthreshold activity at motor nerve endings.” J Physiol 117: 109128.CrossRefGoogle ScholarPubMed
Feynman, R. P., Leighton, R. B., and Sands, M., The Feynman Lectures on Physics. 1963. 4649.CrossRefGoogle Scholar
Fischer, M., et al. (1998). “Rapid actin-based plasticity in dendritic spines.” Neuron 20(5): 847854.CrossRefGoogle ScholarPubMed
Flanagan, L. A., et al. (2002). “Neurite branching on deformable substrates.” Neuroreport 13(18): 24112415.CrossRefGoogle ScholarPubMed
Footer, M. J., et al. (2007). “Direct measurement of force generation by actin filament polymerization using an optical trap.” Proceedings of the National Academy of Sciences of the United States of America 104(7): 21812186.CrossRefGoogle ScholarPubMed
Furukawa, K., et al. (1997). “The actin-severing protein gelsolin modulates calcium channel and NMDA receptor activities and vulnerability to excitotoxicity in hippocampal neurons.” J Neurosci 17(21): 81788186.CrossRefGoogle ScholarPubMed
Gefen, A., et al. (2003). “Age-dependent changes in material properties of the brain and braincase of the rat.” J Neurotrauma 20(11): 11631177.CrossRefGoogle ScholarPubMed
Griesbauer, J., Wixforth, A., and Schneider, M. F.. (2009). “Wave propagation in lipid monolayers.” Biophys J 97(10): 27102716.CrossRefGoogle ScholarPubMed
Halpain, S., Hipolito, A., and Saffer, L.. (1998). “Regulation of F-actin stability in dendritic spines by glutamate receptors and calcineurin.” J Neurosci 18(23): 98359844.CrossRefGoogle ScholarPubMed
Hamill, O. P. and Martinac, B.. (2001). “Molecular basis of mechanotransduction in living cells.” Physiol Rev 81(2): 685740.CrossRefGoogle ScholarPubMed
Heimburg, T. (2010). “Lipid ion channels.” Biophys Chem 150(1–3): 222.CrossRefGoogle ScholarPubMed
Heimburg, T. and Jackson, A. D.. (2005). “On soliton propagation in biomembranes and nerves.” Proc Natl Acad Sci USA 102(28): 97909795.CrossRefGoogle ScholarPubMed
Heimburg, T. and Jackson, A. D.. (2007). “On the action potential as a propagating density pulse and the role of anesthetics.” Biophysical Reviews and Letters 02(01): 5778.CrossRefGoogle Scholar
Hemphill, M. A., et al. (2011). “A possible role for integrin signaling in diffuse axonal injury.” PLoS One 6(7): e22899.CrossRefGoogle ScholarPubMed
Hill, T. L. and Kirschner, M. W.. (1982). “Subunit treadmilling of microtubules or actin in the presence of cellular barriers – possible conversion of chemical free energy into mechanical work.” Proc Natl Acad Sci USA - Biological Sciences 79(2): 490494.CrossRefGoogle ScholarPubMed
Hodgkin, A. L. and Huxley, A. F.. (1952). “A quantitative description of membrane current and its application to conduction and excitation in nerve.” J Physiol 117(4): 500544.CrossRefGoogle ScholarPubMed
Hoge, C. W., et al. (2008). “Mild traumatic brain injury in U.S. Soldiers returning from Iraq.” N Engl J Med 358(5): 453463.CrossRefGoogle ScholarPubMed
Howarth, J. V., et al. (1975). “Heat production associated with passage of a single impulse in pike olfactory nerve-fibers.” Journal of Physiology-London 249(2): 349368.CrossRefGoogle Scholar
Ingber, D. E. (2003). “Tensegrity I. Cell structure and hierarchical systems biology.” J Cell Sci 116(Pt 7): 11571173.CrossRefGoogle ScholarPubMed
Iwasa, K. and Tasaki, I.. (1980). “Mechanical changes in squid giant axons associated with production of action potentials.” Biochem Biophys Res Commun 95(3): 13281331.CrossRefGoogle ScholarPubMed
Jeon, J. and Voth, G. A.. (2005). “The dynamic stress responses to area change in planar lipid bilayer membranes.” Biophys J 88(2): 11041119.CrossRefGoogle ScholarPubMed
Jerabek, H., et al. (2010). “Membrane-mediated effect on ion channels induced by the anesthetic drug ketamine.” J Am Chem Soc 132(23): 79907997.CrossRefGoogle ScholarPubMed
Kilinc, D., Gallo, G., and Barbee, K. A.. (2008). “Mechanically-induced membrane poration causes axonal beading and localized cytoskeletal damage.” Exp Neurol 212(2): 422430.CrossRefGoogle ScholarPubMed
Kim, C. H. and Lisman, J. E.. (1999). “A role of actin filament in synaptic transmission and long-term potentiation.” J Neurosci 19(11): 43144324.CrossRefGoogle ScholarPubMed
Kim, G. H., et al. (2007). “A mechanical spike accompanies the action potential in Mammalian nerve terminals.” Biophys J 92(9): 31223129.CrossRefGoogle ScholarPubMed
Koch, D., et al. (2012). “Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons.” Biophys J 102(3): 452460.CrossRefGoogle ScholarPubMed
Kostic, A., Sap, J., and Sheetz, M. P.. (2007). “RPTPalpha is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons.” J Cell Sci 120(Pt 21): 38953904.CrossRefGoogle ScholarPubMed
Kosztin, I., et al. (2002). “Mechanical force generation by G proteins.” Proc Natl Acad Sci USA 99(6): 35753580.CrossRefGoogle ScholarPubMed
Krucker, T., Siggins, G. R., and Halpain, S.. (2000). “Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus.” Proc Natl Acad Sci USA 97(12): 68566861.CrossRefGoogle ScholarPubMed
Kruse, S. A., et al. (2008). “Magnetic resonance elastography of the brain.” Neuroimage 39(1): 231237.CrossRefGoogle ScholarPubMed
Lamoureux, P., et al. (2002). “Mechanical tension can specify axonal fate in hippocampal neurons.” J Cell Biol 159(3): 499508.CrossRefGoogle ScholarPubMed
Lo, E. H., Wang, X., and Cuzner, M. L.. (2002). “Extracellular proteolysis in brain injury and inflammation: role for plasminogen activators and matrix metalloproteinases.” J Neurosci Res 69(1): 19.CrossRefGoogle ScholarPubMed
Lundstrom, I. (1974). “Mechanical wave propagation on nerve axons.” J Theor Biol 45(2): 487499.CrossRefGoogle ScholarPubMed
Matus, A. (2000). “Actin-based plasticity in dendritic spines.” Science 290(5492): 754758.CrossRefGoogle ScholarPubMed
Matus, A. (2000). “Actin-based plasticity in dendritic spines.” Science 290: 754758.CrossRefGoogle ScholarPubMed
McCracken, P. J., et al. (2005). “Mechanical transient-based magnetic resonance elastography.” Magn Reson Med 53(3): 628639.CrossRefGoogle ScholarPubMed
Meaney, D. F. and Smith, D. H.. (2011). “Biomechanics of concussion.” Clin Sports Med 30(1): 1931, vii.CrossRefGoogle ScholarPubMed
Moore, S. W., Roca-Cusachs, P., and Sheetz, M. P.. (2010). “Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing.” Dev Cell 19(2): 194206.CrossRefGoogle ScholarPubMed
Morris, C. E. (2011). “Voltage-gated channel mechanosensitivity: fact or friction?Front Physiol 2: 25.CrossRefGoogle ScholarPubMed
Murphy, M. C., et al. (2011). “Decreased brain stiffness in Alzheimer’s disease determined by magnetic resonance elastography.” J Magn Reson Imaging 34(3): 494498.CrossRefGoogle ScholarPubMed
Murthy, V. N., et al. (2001). “Inactivity produces increases in neurotransmitter release and synapse size.” Neuron 32(4): 673682.CrossRefGoogle ScholarPubMed
Nguyen, T. D., et al. (2012). “Piezoelectric nanoribbons for monitoring cellular deformations.” Nat Nanotechnol 7(9): 587593.CrossRefGoogle ScholarPubMed
Nordahl, C. W., et al. (2007). “Cortical folding abnormalities in autism revealed by surface-based morphometry.” J Neurosci 27(43): 1172511735.CrossRefGoogle ScholarPubMed
Oh, S., et al. (2012). “Label-free imaging of membrane potential using membrane electromotility.” Biophys J 103(1): 1118.CrossRefGoogle ScholarPubMed
Parekh, S. H., et al. (2005). “Loading history determines the velocity of actin-network growth.” Nat Cell Biol 7(12): 12191223.CrossRefGoogle ScholarPubMed
Pastor, R. W. and Feller, S. E.. (1996). “Time scales of lipid dynamics and molecular dynamics.” Biol Membr 1: 429.Google Scholar
Pekny, M. and Lane, E. B.. (2007). “Intermediate filaments and stress.” Exp Cell Res 313(10): 22442254.CrossRefGoogle ScholarPubMed
Peskin, C. S., Odell, G. M., and Oster, G. F.. (1993). “Cellular motions and thermal fluctuations: the Brownian ratchet.” Biophys J 65(1): 316–24.CrossRefGoogle ScholarPubMed
Petrov, A. G. (2002). “Flexoelectricity of model and living membranes.” Biochim Biophys Acta 1561(1): 125.CrossRefGoogle ScholarPubMed
Petrov, A. G. (2006). “Electricity and mechanics of biomembrane systems: flexoelectricity in living membranes.” Anal Chim Acta 568(1–2): 7083.CrossRefGoogle ScholarPubMed
Pfister, B. J., et al. (2004). “Extreme stretch growth of integrated axons.” J Neurosci 24(36): 79787983.CrossRefGoogle ScholarPubMed
Prange, M. T. and Margulies, S. S.. (2002). “Regional, directional, and age-dependent properties of the brain undergoing large deformation.” J Biomech Eng 124(2): 244252.CrossRefGoogle ScholarPubMed
Reeves, D., et al. (2008). “Membrane mechanics as a probe of ion-channel gating mechanisms.” Physical Review E 78(4): 041901.CrossRefGoogle ScholarPubMed
Rodriguez, O. C., et al. (2003). “Conserved microtubule-actin interactions in cell movement and morphogenesis.” Nat Cell Biol 5(7): 599609.CrossRefGoogle ScholarPubMed
Ronan, L., et al. (2013). “Differential tangential expansion as a mechanism for cortical gyrification.” Cereb Cortex 24(8): 22192228.CrossRefGoogle ScholarPubMed
Roth, S., et al. (2012). “How morphological constraints affect axonal polarity in mouse neurons.” PLoS One 7(3): e33623.CrossRefGoogle ScholarPubMed
Sack, I., et al. (2011). “The influence of physiological aging and atrophy on brain viscoelastic properties in humans.” PLoS One 6(9): e23451.CrossRefGoogle ScholarPubMed
Schikorski, T. and Stevens, C. F.. (1997). “Quantitative ultrastructural analysis of hippocampal excitatory synapses.” J Neurosci 17(15): 58585867.CrossRefGoogle ScholarPubMed
Schliwa, M. and Woehlke, G.. (2003). “Molecular motors.” Nature 422(6933): 759765.CrossRefGoogle ScholarPubMed
Siechen, S., et al. (2009). “Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals.” Proc Natl Acad Sci USA 106(31): 1261112616.CrossRefGoogle ScholarPubMed
Smith, B. A., et al. (2007). “Dendritic spine viscoelasticity and soft-glassy nature: balancing dynamic remodeling with structural stability.” Biophys J 92(4): 14191430.CrossRefGoogle ScholarPubMed
Star, E. N., Kwiatkowski, D. J., and Murthy, V. N.. (2002). “Rapid turnover of actin in dendritic spines and its regulation by activity.” Nat Neurosci 5(3): 239246.CrossRefGoogle ScholarPubMed
Sukharev, S. and Corey, D. P.. (2004). “Mechanosensitive channels: multiplicity of families and gating paradigms.” Sci STKE 2004(219): re4.CrossRefGoogle ScholarPubMed
Tasaki, I. and Byrne, P. M.. (1990). “Volume expansion of nonmyelinated nerve fibers during impulse conduction.” Biophys J 57(3): 633635.CrossRefGoogle ScholarPubMed
Tasaki, I. and Byrne, P. M.. (1992). “Heat production associated with a propagated impulse in bullfrog myelinated nerve fibers.” Jpn J Physiol 42(5): 805813.CrossRefGoogle ScholarPubMed
Tasaki, I., Iwasa, K., and Gibbons, R. C.. (1980). “Mechanical changes in crab nerve fibers during action potentials.” Jpn J Physiol 30(6): 897905.CrossRefGoogle ScholarPubMed
Tasaki, I., Kusano, K., and Byrne, P. M.. (1969). “Rapid mechanical and thermal changes in the garfish olfactory nerve associated with a propagated impulse.” Biophys J 55(6): 10331040.CrossRefGoogle Scholar
Thibault, K. L. and Margulies, S. S.. (1998). “Age-dependent material properties of the porcine cerebrum: effect on pediatric inertial head injury criteria.” J Biomech 31(12): 11191126.CrossRefGoogle ScholarPubMed
Umeda, T., Ebihara, T., and Okabe, S.. (2005). “Simultaneous observation of stably associated presynaptic varicosities and postsynaptic spines: morphological alterations of CA3-CA1 synapses in hippocampal slice cultures.” Mol Cell Neurosci 28(2): 264274.CrossRefGoogle ScholarPubMed
VanEssen, D. C. (1997). “A tension-based theory of morphogenesis and compact wiring in the central nervous system.” Nature 385(6614): 313318.Google Scholar
White, T. and Hilgetag, C. C.. (2011). “Gyrification and neural connectivity in schizophrenia.” Dev Psychopathol 23(1): 339352.CrossRefGoogle ScholarPubMed
Wolf, J. A., et al. (2001). “Traumatic axonal injury induces calcium influx modulated by tetrodotoxin-sensitive sodium channels.” J Neurosci 21(6): 19231930.CrossRefGoogle ScholarPubMed
Wuerfel, J., et al. (2010). “MR-elastography reveals degradation of tissue integrity in multiple sclerosis.” Neuroimage 49(3): 25202525.CrossRefGoogle ScholarPubMed
Xu, G. et al. (2010). “Axons pull on the brain, but tension does not drive cortical folding.” J Biomech Eng 132(7): 071013.CrossRefGoogle Scholar
Xu, G., Bayly, P. V., and Taber, L. A.. (2009). “Residual stress in the adult mouse brain.” Biomech Model Mechanobiol 8(4): 253262.CrossRefGoogle ScholarPubMed
Zhang, J., et al. (2011). “Viscoelastic properties of human cerebellum using magnetic resonance elastography.” Journal of Biomechanics 44(10): 19091913.CrossRefGoogle ScholarPubMed
Zhang, P. C., Keleshian, A. M., and Sachs, F.. (2001). “Voltage-induced membrane movement.” Nature 413(6854): 428432.CrossRefGoogle ScholarPubMed
Zheng, J., et al. (1991). “Tensile regulation of axonal elongation and initiation.” J Neurosci 11(4): 11171125.CrossRefGoogle ScholarPubMed
Zito, K., et al. (2004). “Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton.” Neuron 44(2): 321334.CrossRefGoogle ScholarPubMed
Zohar, O., et al. (1998). “Thermal imaging of receptor-activated heat production in single cells.” Biophys J 74(1): 8289.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×