Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-24T06:44:16.707Z Has data issue: false hasContentIssue false

Multivariate semi-Markov analysis of burst properties of multiconductance single ion channels

Published online by Cambridge University Press:  14 July 2016

F. Ball*
Affiliation:
University of Nottingham
R. K. Milne*
Affiliation:
The University of Western Australia
G. F. Yeo*
Affiliation:
Murdoch University
*
Postal address: School of Mathematical Sciences, The University of Nottingham, Nottingham NG7 2RD, UK.
∗∗ Postal address: Department of Mathematics and Statistics, The University of Western Australia, Crawley, WA 6009, Australia.
∗∗∗ Postal address: Mathematics and Statistics, DSE, Murdoch University, Murdoch, WA 6150, Australia. Email address: [email protected]

Abstract

Patch clamp recordings from ion channels often show periods of repetitive activity, known as bursts, which are noticeably separated from each other by periods of inactivity. Depending on the type of channel, such recordings may exhibit (conductance) levels between the closed (zero) level and the fully open level. Properties of bursts are less subject to problems that arise from recording than are properties for individual sojourns at different levels, and study of bursting behaviour provides important information about the finer structure of the underlying channel gating process. For a general finite state space continuous-time Markov chain model allowing one or more nonzero conductance levels, the present paper establishes results about the semi-Markov structure of a single burst and of a sequence of bursts, and uses this in a unified approach to properties of both theoretical and empirical bursts. The distribution and moments of particular burst properties, including the total charge transfer, the total sojourn time and the total number of visits to specified conductance levels during a burst, are derived. Various extensions are also described.

Type
Research Papers
Copyright
Copyright © Applied Probability Trust 2002 

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

Asmussen, S. (1987). Applied Probability and Queues. John Wiley, Chichester.Google Scholar
Ball, F. (1997). Empirical clustering of bursts of openings in Markov and semi-Markov models of single channel gating incorporating time interval omission. Adv. Appl. Prob. 29, 909946.Google Scholar
Ball, F. (1999). Central limit theorems for multivariate semi-Markov sequences and processes, with applications. J. Appl. Prob. 36, 415432.Google Scholar
Ball, F., and Davies, S. (1997). Clustering of bursts of openings in Markov and semi-Markov models of single channel gating. Adv. Appl. Prob. 29, 92113.Google Scholar
Ball, F., and Sansom, M. (1988). Aggregated Markov processes incorporating time interval omission. Adv. Appl. Prob. 20, 546572.CrossRefGoogle Scholar
Ball, F., Milne, R. K., and Yeo, G. F. (1991). Aggregated semi-Markov processes incorporating time interval omission. Adv. Appl. Prob. 23, 772797.Google Scholar
Ball, F., Milne, R. K., Tame, I. D. and Yeo, G. F. (1997). Superposition of interacting aggregated continuous-time Markov chains. Adv. Appl. Prob. 29, 5691.Google Scholar
Bellman, R. (1970). Introduction to Matrix Analysis, 2nd edn, McGraw-Hill, New York.Google Scholar
Bhat, M. B. et al. (1999). Expression and functional characterization of the cardiac muscle ryanodine receptor Ca2+ release channel in Chinese hamster ovary cells. Biophys. J. 77, 808816.Google Scholar
Colquhoun, D., and Hawkes, A. G. (1982). On the stochastic properties of bursts of single ion channel openings and of clusters of bursts. Phil. Trans. R. Soc. London B 300, 159.Google Scholar
Colquhoun, D., and Hawkes, A. G. (1987). A note on correlations in single ion channel records. Proc. R. Soc. London B 230, 1552.Google Scholar
Colquhoun, D., and Hawkes, A. G. (1990). Stochastic properties of ion channel openings and bursts in a membrane patch that contains two channels: evidence concerning the number of channels present when a record containing only single openings is observed. Proc. R. Soc. London B 240, 453477.Google Scholar
Colquhoun, D., and Hawkes, A. G. (1995). The principles of the stochastic interpretation of ion-channel mechanisms. In Single-Channel Recording, 2nd edn, eds Sakmann, B. and Neher, E., Plenum Press, New York, Chapter 18.Google Scholar
Colquhoun, D., and Sigworth, F. J. (1995). Fitting and statistical analysis of single-channel records. In Single-Channel Recording, 2nd edn, eds Sakmann, B. and Neher, E., Plenum Press, New York, Chapter 19.Google Scholar
Fredkin, D. R., and Rice, J. A. (1986). On aggregated Markov processes. J. Appl. Prob. 23, 208214.CrossRefGoogle Scholar
Hamill, O. P., and Martinac, B. (2001). Molecular basis of mechanotransduction in living cells. Physiol. Rev. 81, 685740.Google Scholar
Hamill, O. P. et al. (1981). Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflüg. Arch. Europ. J. Physiol. 391, 85100.Google Scholar
Hawkes, A. G., Jalali, A., and Colquhoun, D. (1990). The distributions of the apparent open times and shut times in a single channel record when brief events cannot be detected. Phil. Trans. R. Soc. London A 332, 511538.Google Scholar
Janssen, J., and Reinhard, J. M. (1982). Some duality results for a class of multivariate reward processes. J. Appl. Prob. 19, 9098.Google Scholar
Kelly, F. P. (1979). Reversibility and Stochastic Networks. John Wiley, Chichester.Google Scholar
Li, Y. et al. (2000). Burst properties of a supergated double-barrelled chloride ion channel. Math. Biosci. 166, 2344.Google Scholar
McManus, O. B. et al. (1988). Fractal models are inadequate for the kinetics of four different ion channels. Biophys. J. 54, 859870.Google Scholar
Mardia, K. V., Kent, J. T., and Bibby, J. M. (1979). Multivariate Analysis. Academic Press, London.Google Scholar
Ruiz, M. L., and Karpen, J. W. (1997). Single cyclic nucleotide-gated channels locked in different ligand-bound states. Nature 389, 328329.Google Scholar
Saftenku, E., Williams, A. J., and Sitsapesan, R. (2001). Markovian models of low and high activity levels of cardiac ryanodine receptors. Biophys. J. 80, 27272741.CrossRefGoogle ScholarPubMed
Sakmann, B., and Neher, E. (eds) (1995). Single Channel Recording, 2nd edn, Plenum Press, New York.Google Scholar
Sukharev, S. I., Sigurdson, W. J., Kung, C., and Sachs, F. (1999). Energetic and spatial parameters for gating of the bacterial large conductance mechanosensitive channel, MscL. J. Gen. Physiol. 113, 525539.Google Scholar
Yeo, G. F. et al. (2002). Markov modelling of burst behaviour in ion channels. To appear in Handbook of Statistics, Vol. 21, Stochastic Processes: Modelling and Simulation, eds Shanbhag, D. N. and Rao, C. R., North-Holland, Amsterdam.Google Scholar
Zheng, J., and Sigworth, F. J. (1998). Intermediate conductances during deactivation of heteromultimeric Shaker potassium channels. J. Gen. Physiol. 112, 457474.Google Scholar
Zimmermann, H. (1993). Synaptic Transmission: Cellular and Molecular Basis. Georg Thieme Verlag, Stuttgart.Google Scholar