[go: up one dir, main page]
More Web Proxy on the site http://driver.im/ Skip to main content
Springer Nature Link
Log in

The potential and electric field in the cochlear outer hair cell membrane

  • Original Article
  • Published:
Medical & Biological Engineering & Computing Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Outer hair cell electromechanics, critically important to mammalian active hearing, is driven by the cell membrane potential. The membrane protein prestin is a crucial component of the active outer hair cell’s motor. The focus of the paper is the analysis of the local membrane potential and electric field resulting from the interaction of electric charges involved. Here the relevant charges are the ions inside and outside the cell, lipid bilayer charges, and prestin-associated charges (mobile—transferred by the protein under the action of the applied field, and stationary—relatively unmoved by the field). The electric potentials across and along the membrane are computed for the case of an applied DC-field. The local amplitudes and phases of the potential under different frequencies are analyzed for the case of a DC + AC-field. We found that the effect of the system of charges alters the electric potential and internal field, which deviate significantly from their traditional linear and constant distributions. Under DC + AC conditions, the strong frequency dependence of the prestin mobile charge has a relatively small effect on the amplitude and phase of the resulting potential. The obtained results can help in a better understanding and experimental verification of the mechanism of prestin performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
£29.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (United Kingdom)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Ashmore J (1987) A fast motile response in guinea-pig outer hair cell: the cellular basis for cochlear amplifier. J Physiol 388:323–347

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  2. Ashmore J (2004) The cellular machinery in the cochlea. Exp Physiol 79:113–134

    Article  Google Scholar 

  3. Ashmore J, Avan P, Brownell WE, Dallos P, Dierkes K, Fettiplace R, Grosh K, Hackney CM, Hudspeth AJ, Julicher F, Lindner B, Martin P, Meaud J, Petit C, Santos-Sacchi J, Canton B (2010) The remarkable cochlear amplifier. Hear Res 266:1–17

    Article  CAS  PubMed  Google Scholar 

  4. Bai J-P, Surguchev A, Montoya S, Aronson PS, Santos-Sacchi J (2009) Prestin’s anion transport and voltage-sensing capability are independent. Biophys J 96:3179–3185

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Brownell WE, Bader CR, Bertrand D, Ribaupierre Y (1985) Evoked mechanical response of isolated cochlear outer hair cell. Science 227:194–196

    Article  CAS  PubMed  Google Scholar 

  6. Brownell WE, Spector AA, Raphael RM, Popel AS (2001) Micro-and nanomechanics of the cochlear outer hair cell. Annu Rev Biomed Eng 3:169–194

    Article  CAS  PubMed  Google Scholar 

  7. Chen C, Smye SW, Robinson MP, Evans JA (2006) Membrane electroporation theories: a review. Med Biol Eng Comput 44:5–14

    Article  CAS  PubMed  Google Scholar 

  8. Dallos P, Wu X, Cheatham MA, Gao J, Zheng J, Anderson CT, Jia S, Wang X, Cheng WHY, Sengupta S, He DZ, Zuo J (2008) Prestin-based outer hair cell motility is necessary for mammalian cochlear amplification. Neuron 58:333–339

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Deak L, Zheng J, Orem A, Du GG, Aguinaga S, Matsuda K, Dallos P (2005) Effects of cyclic nucleotides on the function of prestin. J. Physiol (London) 563:483–496

    Article  CAS  Google Scholar 

  10. Farrell B, Ugrinov R, Brownell WE (2006) Frequency dependence of admittance and conductance of the outer hair cell. In: Nuttall AL, Ren T, Gillespie PG, Grosh K, de Boer E (eds) Auditory mechanisms, processes, and models. World Scientific, New Jersey, pp 231–232

    Chapter  Google Scholar 

  11. Frank G, Hemmer W, Gummer AW (1999) Limiting dynamics of high-frequency electromechanical transduction of outer hair cells. Proc Natl Acad Sci USA 96:4420–4425

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  12. Gorbunov D, Sturlese M, Nies F, Kluge M, Bellanda M, Battistutta R, Oliver D (2014) Molecular architecture and the structural basis for anion interaction in prestin and SLC26 transporters. Nat Commun 5:3622

    Article  PubMed Central  PubMed  Google Scholar 

  13. Harland B, Brownell WE, Spector AA, Sun SX (2010) Voltage-induced bending and electromechanical coupling in lipid bilayers. Phys Rev E 81:031907

    Article  Google Scholar 

  14. Heimburg T (2012) The capacitance and electromechanical coupling of lipid membranes close to transitions: the effect of electrostriction. Biophys J 103:918–929

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Halter JA, Kruger RP, Yium MJ, Brownell WE (1997) The influence of the subsurface cisterna on the electrical properties of the outer hair cell. Neuroreport 8:2517–2521

    Article  CAS  PubMed  Google Scholar 

  16. Jain MK (1988) Introduction to biological membranes, 2nd edn. Wiley, New York

    Google Scholar 

  17. Johnson SL, Beurg M, Marcotti W, Fettiplace R (2011) Prestin-driven cochlear amplification is not limited by the outer hair cell membrane constant. Neuron 70:1143–1154

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Kralj JM, Hochbaum DR, Douglass AD, Cohen AE (2011) Electrical spiking Escherichia coli probed with a fluorescent voltage-indicating protein. Science 333:345–348

    Article  CAS  PubMed  Google Scholar 

  19. Kralj JM, Douglass AD, Hochbaum DR, Maclaurin D, Cohen AE (2012) Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat Methods 9:90–95

    Article  CAS  Google Scholar 

  20. Liberman MC, Gao J, He DZ, Wu X, Jia S, Zuo J (2002) Prestin is required for electromotility of the outer hair cell and for the cochlear amplifier. Nature 419:300–304

    Article  CAS  PubMed  Google Scholar 

  21. Mosbacher J, Langer M, Horber JKH, Sachs F (1999) Voltage-dependent membrane displacements measured by atomic force microscopy. J Gen Physiol 111:65–74

    Article  Google Scholar 

  22. Mikhopadhyay P, Monicelli L, Tieleman P (2004) Molecular dynamics simulation of a palmitoyl-oleoyl phosphatidylserine bilayer with Na+ counterions and NaCl. Biophys J 86:1601–1609

    Article  Google Scholar 

  23. Mio K, Kubo Y, Ogura T, Yamamoto T, Arisaka F, Sato C (2008) The motor protein prestin is a bullet-shaped molecule with inner cavities. J Biol Chem 283:1137–1145

    Article  CAS  PubMed  Google Scholar 

  24. Muallem D, Ashmore J (2006) An anion antiporter model of prestin, the outer hair cell motor protein. Biophys J 90:4035–4045

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  25. Nakagawa T, Oghalai JS, Saggau P, Rabbitt RD, Brownell WE (2006) Photometric recording of transmembrane potential in outer hair cells. J Neural Eng 3:79–86

    Article  PubMed Central  PubMed  Google Scholar 

  26. Navaratnam D, Bai JP, Samaranayake H, Santos-Sacchi J (2005) N-terminal-mediated homomultimerization of prestin, the outer hair cell motor protein. Biophys J 89:3345–3352

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  27. Oliver D, He DZ, Klocker N, Ludwig J, Schulte U, Waldegger S, Ruppersberg JP, Dallos P, Fakler B (2001) Inracellular anions as the voltage sensor of prestin, the outer hair cell motor protein. Science 292:2340–2443

    Article  CAS  PubMed  Google Scholar 

  28. Pandit S, Berkovitz M (2002) Molecular dynamics simulation of dipalmitoylphosphatidylserine bilayer with Na+ counterions. Biophys J 82:1818–1827

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Pandit S, Bostick D, Berkovitz M (2003) Molecular dynamics simulation of a dipalmitoylphosphatidylcholine bilayer with NaCl. Biophys J 84:3743–3750

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  30. Petrov AG (1999) The lyotropic state of matter: molecular physics and living matter physics. Gordon & Breach Science Publishers, Sydney

    Google Scholar 

  31. Rybalchenko V, Santos-Sacchi J (2003) Cl− flux through a non-selective, stretch-sensitive conductance influences the outer hair cell motor of the guinea pig. J Physiol (London) 547:873–891

    Article  CAS  Google Scholar 

  32. Santos-Sacchi J, Dilger JP (1988) Whole cell currents and mechanical response of isolated outer hair cell. Hear Res 35:143–150

    Article  CAS  PubMed  Google Scholar 

  33. Schaechinger TJ, Oliver D (2007) Nonmammalian orthologs of prestin (SLC26A5) are electrogenic divalent/chloride anion exchangers. Proc Natl Acad Sci USA 104:7693–7696

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Silver BL (1985) The physical chemistry of membranes. The Solomon Press, New York

    Book  Google Scholar 

  35. Song L, Santos-Sacchi J (2010) Conformational state-dependent anion binding in prestin: evidence for allosteric modulation. Biophys J 98:371–376

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Song L, Santos-Sacchi J (2011) Chloride dependent coupling of molecular to cellular mechanics in the outer hair cell of Corti’s organ. In: Shera CA, Olson ES (eds) What fire is in mine ears: progress in auditory biomechanics. American Institute of Physics, Melville, pp 179–184

    Google Scholar 

  37. Spector AA, Brownell WE, Popel AS (1999) Mechanical and electromotile characteristics of auditory outer hair cells. Med Biol Eng Comput 37:247–251

    Article  CAS  PubMed  Google Scholar 

  38. Sun SX, Farrell B, Chana MS, Oster G, Brownell WE, Spector AA (2009) Voltage and frequency dependence of prestin-associated charge transfer. J Theor Biol 260:137–144

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  39. Tofts PS, Branston NM (1991) The measurement of electric field, and the influence of surface charge, in magnetic stimulation. Electroencephalogr Clin Neurophysiol 81:238–239

    Article  CAS  PubMed  Google Scholar 

  40. Ye H, Cotic M, Fehlings MG, Carden PL (2011) Transmembrane potential generated by a magnetically induced transverse electric field in a cylindrical axonal model. Med Biol Eng Comput 49:107–119

    Article  PubMed  Google Scholar 

  41. Zheng J, Shen W, He DZ, Long KB, Madison LD, Dallos P (2000) Prestin is the motor protein of cochlear outer hair cells. Nature 405:149–155

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by research Grant R01 DC 000354 from National Institute of Deafness and Other Communication Disorders (NIH).

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, Johns Hopkins University, Baltimore, MD, 21218, USA

    Ben Harland, Sean X. Sun & Alexander A. Spector

  2. Department of Biomedical Engineering, Johns Hopkins University, Baltimore, MD, 21205, USA

    Wen-han Lee, Sean X. Sun & Alexander A. Spector

  3. Bobby R. Alford Department of Otolaryngology, Head and Neck Surgery, Baylor College of Medicine, Houston, TX, 77030, USA

    William E. Brownell

Authors
  1. Ben Harland
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wen-han Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. William E. Brownell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sean X. Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alexander A. Spector
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alexander A. Spector.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Harland, B., Lee, Wh., Brownell, W.E. et al. The potential and electric field in the cochlear outer hair cell membrane. Med Biol Eng Comput 53, 405–413 (2015). https://doi.org/10.1007/s11517-015-1248-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11517-015-1248-0

Keywords

Search

Navigation