{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,5]],"date-time":"2026-07-05T02:36:03Z","timestamp":1783218963210,"version":"3.54.6"},"reference-count":48,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2013,6,6]],"date-time":"2013-06-06T00:00:00Z","timestamp":1370476800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/3.0\/"},{"start":{"date-parts":[[2013,6,6]],"date-time":"2013-06-06T00:00:00Z","timestamp":1370476800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/3.0\/"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"DOI":"10.1038\/srep01956","type":"journal-article","created":{"date-parts":[[2013,6,6]],"date-time":"2013-06-06T09:13:08Z","timestamp":1370509988000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Breakup and then makeup: a predictive model of how cilia self-regulate hardness for posture control"],"prefix":"10.1038","volume":"3","author":[{"given":"Promode R.","family":"Bandyopadhyay","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joshua C.","family":"Hansen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2013,6,6]]},"reference":[{"key":"BFsrep01956_CR1","doi-asserted-by":"crossref","first-page":"2537","DOI":"10.1242\/jeb.198.12.2537","volume":"198","author":"J Pernberg","year":"1995","unstructured":"Pernberg, J. & Machemer, H. Voltage-dependence of ciliary activity in the ciliate Didinium nasutum. J. Exp. Biol. 198, 2537\u20132545 (1995).","journal-title":"J. Exp. Biol."},{"key":"BFsrep01956_CR2","doi-asserted-by":"publisher","first-page":"451","DOI":"10.1083\/jcb.78.2.451","volume":"78","author":"R Dute","year":"1978","unstructured":"Dute, R. & Kung, C. Ultrastructure of the proximal region of somatic cilia in paramecium tetraurelia. J. Cell Biol. 78, 451\u2013464 (1978).","journal-title":"J. Cell Biol."},{"key":"BFsrep01956_CR3","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1242\/jeb.57.1.239","volume":"57","author":"H Machemer","year":"1972","unstructured":"Machemer, H. Ciliary activity and the origin of metachrony in paramecium: effects of increased viscosity. J. Exp. Biol. 57, 239\u2013259 (1972).","journal-title":"J. Exp. Biol."},{"key":"BFsrep01956_CR4","doi-asserted-by":"publisher","first-page":"381","DOI":"10.1016\/S0006-3495(94)80493-X","volume":"67","author":"PMF Teunis","year":"1994","unstructured":"Teunis, P. M. F. & Machemer, H. Analysis of three-dimensional ciliary beating by means of high-speed stereomicroscopy. Biophys. J. 67, 381\u2013394 (1994).","journal-title":"Biophys. J."},{"key":"BFsrep01956_CR5","doi-asserted-by":"publisher","first-page":"1128","DOI":"10.1038\/srep01128","volume":"3","author":"PR Bandyopadhyay","year":"2013","unstructured":"Bandyopadhyay, P. R., Leinhos, H. A. & Hellum, A. M. Handedness helps homing in swimming and flying animals. Sci. Rep. 3, 1128, 10.1038\/srep01128 (2013).","journal-title":"Sci. Rep."},{"key":"BFsrep01956_CR6","doi-asserted-by":"publisher","first-page":"298","DOI":"10.1017\/jfm.2012.178","volume":"702","author":"PR Bandyopadhyay","year":"2012","unstructured":"Bandyopadhyay, P. R., Beal, D. N., Hrubes, J. D. A. & Mangalam, A. Relationship of roll and pitch oscillations in a fin flapping at transitional to high Reynolds numbers. J. Fluid Mech. 702, 298\u2013331 (2012).","journal-title":"J. Fluid Mech."},{"key":"BFsrep01956_CR7","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1186\/gm275","volume":"3","author":"JE Lee","year":"2011","unstructured":"Lee, J. E. & Gleeson, J. G. A systems-biology approach to understanding the ciliopathy disorders. Genome Med. 3 (9), 59, 10.1186\/gm275 (2011).","journal-title":"Genome Med."},{"key":"BFsrep01956_CR8","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1038\/276285a0","volume":"276","author":"J dePeyer","year":"1978","unstructured":"dePeyer, J. & Machemer, H. Are receptor-activated ciliary motor responses mediated through voltage or current? Nature 276, 285\u2013287 (1978).","journal-title":"Nature"},{"key":"BFsrep01956_CR9","doi-asserted-by":"publisher","first-page":"15670","DOI":"10.1073\/pnas.1005127107","volume":"107","author":"AR Shields","year":"2010","unstructured":"Shields, A. R. et al. Biomimetic cilia arrays generate simultaneous pumping and mixing regimes. Proc. Nat. Acad. Sci. 107 (36), 15670\u201315675 (2010).","journal-title":"Proc. Nat. Acad. Sci."},{"key":"BFsrep01956_CR10","doi-asserted-by":"publisher","first-page":"6001","DOI":"10.1073\/pnas.94.12.6001","volume":"94","author":"S Gueron","year":"1997","unstructured":"Gueron, S., Levit-Gurevich, K., Liron, N. & Blum, J. J. Cilia internal mechanism and metachronal coordination as the result of hydrodynamical coupling. Proc. Natl. Acad. Sci. USA, 94, 6001\u20136006 (1997).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"BFsrep01956_CR11","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1146\/annurev.genom.7.080505.115610","volume":"7","author":"JL Badano","year":"2006","unstructured":"Badano, J. L., Mitsuma, N., Beales, P. L. & Katsanis, N. The ciliopathies: an emerging class of human genetic disorders. Ann. Rev. Genom. Hum. Gen. 7, 125\u2013148, 10.1146\/annurev.genom.7.080505.115610 (2006).","journal-title":"Ann. Rev. Genom. Hum. Gen."},{"key":"BFsrep01956_CR12","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1242\/jeb.200.3.583","volume":"200","author":"JM Wakeling","year":"1997","unstructured":"Wakeling, J. M. & Ellington, C. P. Dragonfly flight, III. Lift and power requirements. J. Exp. Biol. 200, 583\u2013600 (1997).","journal-title":"J. Exp. Biol."},{"key":"BFsrep01956_CR13","doi-asserted-by":"publisher","first-page":"549","DOI":"10.1113\/jphysiol.1981.sp013763","volume":"315","author":"RR Llinas","year":"1981","unstructured":"Llinas, R. R. & Yarom, Y. Electrophysiology of mammalian inferior-olive neurons in vitro, different types of voltage dependences in conductances. J. Phys. (London) 315, 549\u2013567 (1981).","journal-title":"J. Phys. (London)"},{"key":"BFsrep01956_CR14","doi-asserted-by":"crossref","unstructured":"Llinas, R. R. I of the Vortex from Neurons to Self (MIT Press, CambridgeMA) (2001).","DOI":"10.7551\/mitpress\/3626.001.0001"},{"key":"BFsrep01956_CR15","doi-asserted-by":"publisher","first-page":"797","DOI":"10.1016\/j.neuroscience.2009.04.045","volume":"162","author":"RR Llinas","year":"2009","unstructured":"Llinas, R. R. Inferior olive oscillation as the temporal basis for motricity and oscillatory reset as the basis for motor error correction. Neuroscience 162 (3), 797\u2013804 (2009).","journal-title":"Neuroscience"},{"key":"BFsrep01956_CR16","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1038\/nrn2756","volume":"11","author":"P Dean","year":"2010","unstructured":"Dean, P., Porril, J., Ekerot, C-F. & Jornteli, H. The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat. Rev.: Neurosci. 11, 30\u201343 (2010).","journal-title":"Nat. Rev.: Neurosci."},{"key":"BFsrep01956_CR17","doi-asserted-by":"publisher","first-page":"631","DOI":"10.1109\/JOE.2004.833212","volume":"29","author":"RR Llinas","year":"2004","unstructured":"Llinas, R. R., Leznik, E. & Makarenko, V. I. The olivo-cerebellar circuit as a universal control system. IEEE J. Oceanic Engrg. 29, 631\u2013639 (2004).","journal-title":"IEEE J. Oceanic Engrg."},{"key":"BFsrep01956_CR18","doi-asserted-by":"publisher","first-page":"13064","DOI":"10.1073\/pnas.1635110100","volume":"100","author":"VB Kazantsev","year":"2003","unstructured":"Kazantsev, V. B., Nekorkin, V., Makarenko, V. & Llinas, R. Olivo-cerebellar cluster-based universal control system. Proc. Nat. Acad. Sci. 100 (22), 13064\u201313068 (2003).","journal-title":"Proc. Nat. Acad. Sci."},{"key":"BFsrep01956_CR19","doi-asserted-by":"publisher","first-page":"18183","DOI":"10.1073\/pnas.0407900101","volume":"101","author":"VB Kazantsev","year":"2004","unstructured":"Kazantsev, V. B., Nekorkin, V., Makarenko, V. & Llinas, R. Self-referential phase reset based on inferior olive oscillator dynamics. Proc. Nat. Acad. Sci. 101, 18183\u201318188 (2004).","journal-title":"Proc. Nat. Acad. Sci."},{"key":"BFsrep01956_CR20","doi-asserted-by":"publisher","first-page":"223","DOI":"10.1007\/BF00606372","volume":"150","author":"JE dePeyer","year":"1983","unstructured":"dePeyer, J. E. & Machemer, H. Threshold activation and dynamic response range of cilia following low rates of membrane polarization under voltage-clamp. J. Comp. Physiology 150, 223\u2013232 (1983).","journal-title":"J. Comp. Physiology"},{"key":"BFsrep01956_CR21","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1242\/jcs.65.1.223","volume":"65","author":"Y Nakaoka","year":"1984","unstructured":"Nakaoka, Y., Tanaka, H. & Oosawa, F. Ca2+-dependent regulation of beat frequency of cilia in paramecium. J. Cell. Science 65, 223\u2013231 (1984).","journal-title":"J. Cell. Science"},{"key":"BFsrep01956_CR22","doi-asserted-by":"publisher","first-page":"113","DOI":"10.1007\/BF00605396","volume":"154","author":"JW Deitmer","year":"1984","unstructured":"Deitmer, J. W., Machemer, H. & Martinac, B. Motor control in three types of ciliary organelles in the ciliate stylonychia. J. Comp. Physiology A 154, 113\u2013120 (1984).","journal-title":"J. Comp. Physiology A"},{"key":"BFsrep01956_CR23","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1038\/ncb2040","volume":"12","author":"B Guirao","year":"2010","unstructured":"Guirao, B. et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat. Cell. Biol. 12, 341\u2013350 (2010).","journal-title":"Nat. Cell. Biol."},{"key":"BFsrep01956_CR24","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1042\/BC20060031","volume":"99","author":"LF Jaffe","year":"2007","unstructured":"Jaffe, L. F. Stretch-activated calcium channels relay fast calcium waves propagated by calcium-induced calcium influx. Biol. Cell. 99, 175\u2013184, 10.1042\/BC20060031 (2007).","journal-title":"Biol. Cell."},{"key":"BFsrep01956_CR25","unstructured":"Khalil, H. K. Nonlinear Systems (Prentice-Hall, Upper-Saddle RiverNJ) (1996)."},{"key":"BFsrep01956_CR26","unstructured":"Slotine, J.-J. E. & Li, W. Applied Nonlinear Control (Prentice-Hall, Englewood CliffsNJ), pp. 160\u2013163 (1991)."},{"key":"BFsrep01956_CR27","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1109\/JOE.2008.2005356","volume":"33","author":"PR Bandyopadhyay","year":"2008","unstructured":"Bandyopadhyay, P. R. et al. Synchronization of animal-inspired multiple fins in an underwater vehicle using olivo-cerebellar dynamics. IEEE J. Oceanic Engrg. 33(4), 563\u2013578 (2008).","journal-title":"IEEE J. Oceanic Engrg."},{"key":"BFsrep01956_CR28","doi-asserted-by":"crossref","unstructured":"Zwillinger, D. Standard Mathematical Tables and Formulae (CRC Press) (1996).","DOI":"10.1201\/9781003040965"},{"key":"BFsrep01956_CR29","doi-asserted-by":"publisher","first-page":"339","DOI":"10.1073\/pnas.89.1.339","volume":"89","author":"NJ Cordova","year":"1992","unstructured":"Cordova, N. J., Ermentrout, B. and Oster, G. F. Dynamics of single-motor molecules: the thermal ratchet model. Proc. Nat. Acad. Sci. Biophys. 89, 339\u2013343 (1992).","journal-title":"Proc. Nat. Acad. Sci. Biophys."},{"key":"BFsrep01956_CR30","unstructured":"Karp, G. Cell and Molecular Biology: Concepts and Experiments 4th Edition (John Wiley and Sons, HobokenNJ), 346\u2013358 (2005)."},{"key":"BFsrep01956_CR31","first-page":"163","volume":"A221","author":"AA Griffith","year":"1920","unstructured":"Griffith, A. A. The phenomena of rupture and flow in solids. Phil. Trans. Roy. Soc. A221, 163\u2013198 (1920).","journal-title":"Phil. Trans. Roy. Soc."},{"key":"BFsrep01956_CR32","unstructured":"Irwin, G. R. Fracture Dynamics, in Fracturing of Metals. (Amer. Soc. Metals, Cleveland, OH), pp. 147\u2013166 (1948)."},{"key":"BFsrep01956_CR33","doi-asserted-by":"publisher","first-page":"3779","DOI":"10.1529\/biophysj.107.122028","volume":"94","author":"I Adamovic","year":"2008","unstructured":"Adamovic, I., Mijailovich, S. M. & Karplus, M. The elastic properties of the structurally characterized Myosin II S2 subdomain: a molecular dynamics and normal mode analysis. Biophysics J. 94, 3779\u20133789 (2008).","journal-title":"Biophysics J."},{"key":"BFsrep01956_CR34","doi-asserted-by":"publisher","first-page":"094014","DOI":"10.1088\/0964-1726\/20\/9\/094014","volume":"20","author":"GV Lauder","year":"2011","unstructured":"Lauder, G. V., Madden, P. G. A., Tangora, J. L., Anderson, E. & Baker, T. V. Bioinspiration from fish for smart material design and function. Smart Materials and Structures 20, 094014 (2011).","journal-title":"Smart Materials and Structures"},{"key":"BFsrep01956_CR35","doi-asserted-by":"publisher","first-page":"13051","DOI":"10.1073\/pnas.0601839103","volume":"103","author":"K Guevorkian","year":"2006","unstructured":"Guevorkian, K. & Valles, J. M. Swimming paramecium in magnetically simulated enhanced, reduced and inverted gravity environments. Proc. Nat. Acad. Sci. 103(35), 13051\u201313056 (2006).","journal-title":"Proc. Nat. Acad. Sci."},{"key":"BFsrep01956_CR36","doi-asserted-by":"publisher","first-page":"8620870","DOI":"10.1242\/jeb.051151","volume":"214","author":"C Spoon","year":"2011","unstructured":"Spoon, C. & Grant, W. Biomechanics of hair cell kinocilia: experimental measurement of kinocilium shaft stiffness and base rotational stiffness with Euler-Bernoulli and Timoshenko beam analysis. J. Exp. Biol. 214, 8620870 (2011).","journal-title":"J. Exp. Biol."},{"key":"BFsrep01956_CR37","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1006\/jtbi.1994.1221","volume":"171","author":"JE Schoutens","year":"1994","unstructured":"Schoutens, J. E. Prediction of elastic properties of sperm flagella. J. Theor. Bio. 171, 163\u2013177 (1994).","journal-title":"J. Theor. Bio."},{"key":"BFsrep01956_CR38","unstructured":"Thompson, W. T. & Dahleh, M. D. Theory of Vibration, 5th Edition (Prentice Hall) (1993)."},{"key":"BFsrep01956_CR39","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1007\/BF01766492","volume":"11","author":"Y Yeh","year":"1990","unstructured":"Yeh, Y., Baskin, R. J., Shen, S. & Jones, M. Photon correlation spectroscopy of the polarization signal of single muscle fibers. J. Muscle Research and Cell Motility 11 (2), 137\u2013146 (1990).","journal-title":"J. Muscle Research and Cell Motility"},{"key":"BFsrep01956_CR40","doi-asserted-by":"publisher","first-page":"6987","DOI":"10.1073\/pnas.86.18.6987","volume":"86","author":"SL Tamm","year":"1989","unstructured":"Tamm, S. L. & Tamm, S. Calcium sensitivity extends the length of ATP-reactivated ciliary axonemes. Proc. Nat. Acad. Sciences, Cell Biology 86, 6987\u20136991 (1989).","journal-title":"Proc. Nat. Acad. Sciences, Cell Biology"},{"key":"BFsrep01956_CR41","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1242\/jeb.25.2.123","volume":"25","author":"BA Humphrey","year":"1948","unstructured":"Humphrey, B. A. & Humphrey, G. F. Studies in the respiration of Paramecium caudatum. J. Exp. Biol. 25(2), 123\u201334 (1948).","journal-title":"J. Exp. Biol."},{"key":"BFsrep01956_CR42","unstructured":"Roberts, M. B. V. Biology: A Functional Approach. 4th edition (Thomas Nelson Publ., CheltenhamUK) (1986)."},{"key":"BFsrep01956_CR43","doi-asserted-by":"crossref","unstructured":"Bandyopadhyay, P. R. & Leinhos, H. A. Propulsion efficiency of bodies appended with multiple flapping fins \u2013 when more is less. Phys. Fl. 25, 041902, http:\/\/dx.doi.org\/10.1063\/1.4802495 (2013).","DOI":"10.1063\/1.4802495"},{"key":"BFsrep01956_CR44","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1017\/S0022112004008468","volume":"506","author":"N Vandenberghe","year":"2004","unstructured":"Vandenberghe, N., Zhang, J. and Childress, S. Symmetry breaking leads to forward flapping flight. J. Fluid Mech. 506, 147\u2013155 (2004).","journal-title":"J. Fluid Mech."},{"key":"BFsrep01956_CR45","doi-asserted-by":"publisher","first-page":"415","DOI":"10.1006\/jtbi.2000.2182","volume":"207","author":"RH Dillon","year":"2000","unstructured":"Dillon, R. H. & Fauci, L. J. An integrative model of internal axoneme mechanics and external fluid dynamics in ciliary beating. J. Theo. Biol. 207, 415\u2013430 (2000).","journal-title":"J. Theo."},{"key":"BFsrep01956_CR46","doi-asserted-by":"publisher","first-page":"599","DOI":"10.1098\/rspb.2000.1396","volume":"268","author":"S Gueron","year":"2001","unstructured":"Gueron, S. & Levit-Gurevich, K. A three-dimensional model for ciliary motion based on the internal 9 + 2 structure. Proc. Roy. Soc. Lond. B 268, 599\u2013607 (2001).","journal-title":"Proc. Roy. Soc. Lond. B"},{"key":"BFsrep01956_CR47","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1142\/S0218127400000840","volume":"10","author":"EM Izhikevich","year":"2000","unstructured":"Izhikevich, E. M. Neural excitability, spiking and bursting. Int. J. Bifurcation and Chaos 10(6), 1171\u20131266 (2000).","journal-title":"Int. J. Bifurcation and Chaos"},{"key":"BFsrep01956_CR48","doi-asserted-by":"publisher","first-page":"024501","DOI":"10.1115\/1.4000766","volume":"132","author":"K Kongthon","year":"2010","unstructured":"Kongthon, K. et al. Added-mass effect in modeling of cilia-based devices for microfluidic systems. Trans. ASME J. Vibr. Acou. 132, 024501\u20131 (7p) (2010).","journal-title":"Trans. ASME J. Vibr. Acou."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/srep01956","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep01956.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/srep01956.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,6]],"date-time":"2023-01-06T05:38:00Z","timestamp":1672983480000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/srep01956"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2013,6,6]]},"references-count":48,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2013,12,20]]}},"alternative-id":["BFsrep01956"],"URL":"https:\/\/doi.org\/10.1038\/srep01956","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,6,6]]},"assertion":[{"value":"4 March 2013","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 May 2013","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 June 2013","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1956"}}