Skip to main content
Log in

A model of signal processing at the isolated hair cell of the frog semicircular canal

  • Published:
Journal of Computational Neuroscience Aims and scope Submit manuscript

Abstract

A computational model has been developed to simulate the electrical behavior of the type II hair cell dissected from the crista ampullaris of frog semicircular canals. In its basolateral membrane, it hosts a system of four voltage-dependent conductances (g A , g KV , g KCa , g Ca ). The conductance behavior was mathematically described using original patch-clamp experimental data. The transient K current, IA, was isolated as the difference between the currents obtained before and after removing IA inactivation. The remaining current, IKD, results from the summation of a voltage-dependent K current, IKV, a voltage-calcium-dependent K current, IKCa, and the calcium current, ICa. IKD was modeled as a single lumped current, since the physiological role of each component is actually not discernible. To gain a clear understanding of its prominent role in sustaining transmitter release at the cytoneural junction, ICa was modeled under different experimental conditions. The model includes the description of voltage- and time-dependent kinetics for each single current. After imposing any starting holding potential, the system sets the pertinent values of the variables and continually updates them in response to variations in membrane potential. The model reconstructs the individual I-V curves obtained in voltage-clamp experiments and simulations compare favorably with the experimental data. The model proves useful in describing the early steps of signal processing that results from the interaction of the apical receptor current with the basolateral voltage-dependent conductances. The program is thus helpful in understanding aspects of sensory transduction that are hard to analyze in the native hair cell of the crista ampullaris.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexandrov, V. V., Alexandrova, T. B., Astakhova, T. G., Kulikovskaya, N. V., Kurilov, V. I., Migunov, S. S., Shulenina, N. E., Soto, E., & Vega, R. (2004). A mathematical model of the response of semicircular canal and otolith to head rotation under gravity. Journal of Gravitational Physiology, 11, 25–26.

    Google Scholar 

  • Art, J. J., & Fettiplace, R. (1987). Variation of membrane properties in hair cells isolated from the turtle cochlea. The Journal of Physiology, 385, 207–242.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boyle, R., Rabbitt, R. D., & Highstein, M. (2009). Efferent control of hair cell and afferent response in the semicircular canals. Journal of Neurophysiology, 102, 1513–1525. doi:10.1152/jn.91367.2008.

    Article  PubMed  PubMed Central  Google Scholar 

  • Deka, K. M., & Roy, S. (2014). Glutamate gated spiking Neuron model. Annals of Neurosciences, 21, 14–18. doi:10.5214/ans.0972.7531.210105.

    PubMed  PubMed Central  Google Scholar 

  • Galtier, M. N., & Touboul, J. (2013). Macroscopic equations governing noisy spiking neuronal populations with linear synapses. PLoS ONE, 8, e78917. doi:10.1371/journal.pone.0078917.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gillespie, P. G., & Muller, U. (2009). Mechanotransduction by hair cells: models, molecules and mechanisms. Cell, 139, 33–44. doi:10.1016/j.cell.2009.09.010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodman, M. B., & Art, J. J. (1996). Positive feedback by a potassium-selective inward rectifier enhances tuning in vertebrate hair cells. Biophysical Journal, 71, 430–442.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagiwara, S., & Byerly, L. (1981). Calcium channels. Annual Review of Neuroscience, 4, 69–125.

    Article  CAS  PubMed  Google Scholar 

  • Hodgkin, A. L., & Huxley, A. F. (1952). A quantitative description of membrane currents and its application to conduction and excitation in nerve. Journal of Physiology (London), 117, 500–544.

    Article  CAS  Google Scholar 

  • Housley, G. D., Noms, C. H., & Guth, P. S. (1989). Electrophysiological properties and morphology of hair cells isolated from the semicircular canal of the frog. Hearing Research, 38, 259–276.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, B. A., & Lansner, A. (2014). A spiking neural network model of self-organized pattern recognition in the early mammalian olfactory system. Frontiers in Neural Circuits, 8, 5. doi:10.3389/fncir.2014.00005.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez-Poveda, E. A., & Eustatio-Martin, A. (2006). A biophysical model of the inner hair cell: the contribution of potassium currents to peripheral auditory compression. JARO, 7, 218–235. doi:10.1007/s10162-006-0037-8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Martini, M., Rossi, M. L., Rubbini, G., & Rispoli, G. (2000). Calcium currents in hair cells isolated from semicircular canals of the frog. Biophysical Journal, 78, 1240–1254. doi:10.1016/S0006-3495(00)76681-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martini M, Farinelli F, Rossi ML, Rispoli G. (2007). Ca2+ current of frog vestibular hair cells is modulated by intracellular ATP but not by long-lasting depolarisation. European Biophysics Journal, 36(7):779–86.

  • Martini, M., Canella, R., Fesce, R., & Rossi, M. L. (2009a). Isolation and possible role of fast and slow potassium current components in hair cells dissociated from frog crista ampullaris. Pflügers Archiv, 457, 1327–1342. doi:10.1007/s00424-008-0598-y.

    Article  CAS  PubMed  Google Scholar 

  • Martini, M., Canella, R., Leparulo, A., Prigioni, I., Fesce, R., & Rossi, M. L. (2009b). Ionic currents in hair cells dissociated from frog semicircular canals after preconditioning under microgravity conditions. American Journal of Physiology, 296, 1585–1597. doi:10.1152/ajpregu.90981.2008.

    Google Scholar 

  • Martini, M., Canella, R., Fesce, R., & Rossi, M. L. (2013). The amplitude and inactivation properties of the delayed potassium currents are regulated by protein kinase activity in hair cells of the frog semicircular canals. PLoS ONE, 8, e67784. doi:10.1371/journal.pone.0067784.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martini, M., Canella, R., Rubbini, G., Fesce, R., & Rossi, M. L. (2015). Sensory transduction at the frog semicircular canal: how hair cell membrane potential controls junctional transmission. Frontiers in Cellular Neuroscience, 9, 1–17. doi:10.3389/fncel.2015.00235.

    Article  Google Scholar 

  • Neiman, A. B., Dierkes, K., Lindner, B., Han, L., & Shilnikov, A. L. (2011). Spontaneous voltage oscillations and response dynamics of a Hodgkin-Huxley type model of sensory hair cells. Journal of Mathematical Neuroscience, 1, 11. doi:10.1186/2190-8567-1-11.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rabbitt, R. D., Boyle, R., Holstein, G. R., & Highstein, S. M. (2004). Hair-cell versus afferent adaptation in the semicircular canals. Journal of Neurophysiology, 93, 424–436. doi:10.1152/jn.00426.2004.

    Article  PubMed  PubMed Central  Google Scholar 

  • Soto, E., Vega, R., & Budelli, R. (2002). The receptor potential in type I and T type II vestibular system hair cells: a model analysis. Hearing Research, 165, 35–47.

    Article  CAS  PubMed  Google Scholar 

  • Zeddies, D. G., & Siegel, J. H. (2004). A biophysical model of an inner hair cell. The Journal of Acoustical Society of America, 116, 426–441.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Profs. O. Sacchi and O. Belluzzi for helpful comments on the manuscript and Drs. M. Sandri and A. Pignatelli for support in program implementation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rita Canella.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Action Editor: Israel Nelken

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Canella, R., Martini, M. & Rossi, M.L. A model of signal processing at the isolated hair cell of the frog semicircular canal. J Comput Neurosci 42, 123–131 (2017). https://doi.org/10.1007/s10827-016-0631-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10827-016-0631-7

Keywords

Navigation