Study on the temperature characteristics of fast capacitance in patch clamp experiments_Journal of Biomedical Engineering

Authors：

KONG Fanyi ¹ , LI Xinyu ² , JIAO Ruonan ¹ ,  SUN Changsen ¹

1. Biomedical Optics Laboratory, School of Optoelectronic Engineering and Instrumentation Science, Dalian University of Technology, Dalian, Liaoning 116000, P.R.China;
2. School of Electronics and Information Technology, Sun Yat-sen University, Guangzhou 510006, P.R.China;

Corresponding?author：

SUN Changsen, Email: suncs@dlut.edu.cn

Keywords：

fast capacitance; fast capacitance compensation; fast capacitance temperature characteristic; patch clamp

DOI：

10.7507/1001-5515.202007054

Video：

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Patch clamp is a technique that can measure weak current in the level of picoampere (pA). It has been widely used for cellular electrophysiological recording in fundamental medical researches, such as membrane potential and ion channel currents recording, etc. In order to obtain accurate measurement results, both the resistance and capacitance of the pipette are required to be compensated. Capacitance compensations are composed of slow and fast capacitance compensation. The slow compensation is determined by the lipid bilayer of cell membrane, and its magnitude usually ranges from a few picofarads (pF) to a few microfarads (μF), depending on the cell size. The fast capacitance is formed by the distributed capacitance of the glass pipette, wires and solution, mostly ranging in a few picofarads. After the pipette sucks the cells in the solution, the positions of the glass pipette and wire have been determined, and only taking once compensation for slow and fast capacitance will meet the recording requirements. However, when the study needs to deal with the temperature characteristics, it is still necessary to make a recognition on the temperature characteristic of the capacitance. We found that the time constant of fast capacitance discharge changed with increasing temperature of bath solution when we studied the photothermal effect on cell membrane by patch clamp. Based on this phenomenon, we proposed an equivalent circuit to calculate the temperature-dependent parameters. Experimental results showed that the fast capacitance increased in a positive rate of 0.04 pF/℃, while the pipette resistance decreased. The fine data analysis demonstrated that the temperature rises of bath solution determined the kinetics of the fast capacitance mainly by changing the inner solution resistance of the glass pipette. This result will provide a good reference for the fine temperature characteristic study related to cellular electrophysiology based on patch clamp technique.

Citation： KONG Fanyi, LI Xinyu, JIAO Ruonan, SUN Changsen. Study on the temperature characteristics of fast capacitance in patch clamp experiments. Journal of Biomedical Engineering, 2021, 38(4): 695-702. doi: 10.7507/1001-5515.202007054 Copy

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2.	Hodgkin A L, Huxley A F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol, 1952, 117(4): 500-544.
3.	Hodgkin A L, Huxley A F, Katz B. Measurement of current-voltage relations in the membrane of the giant axon of loligo. J Physiol London, 1952, 116(4): 424-448.
4.	Anderson C R, Cull-Candy S G, Miledi R. Potential-dependent transition temperature of ionic channels induced by glutamate in locust muscle. Nature, 1977, 268(5621): 663-665.
5.	Paris L, Marc I, Charlot B, et al. Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons. Biomed Opt Express, 2017, 8(10): 4568-4578.
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13.	Shapiro M G, Homma K, Villarreal S, et al. Infrared light excites cells by changing their electrical capacitance. Nat Commun, 2012, 3: 736.
14.	Li Xinyu, Liu Jia, Liang Shanshan, et al. 980-Nm infrared laser modulation of sodium channel kinetics in a neuron cell linearly mediated by photothermal effect. J Biomed Opt, 2014, 19(10): 105002.
15.	Shapiro M G, Priest M F, Siegel P H, et al. Thermal mechanisms of millimeter wave stimulation of excitable cells. Biophys J, 2013, 104(12): 2622-2628.
16.	Yao Jing, Liu Beiying, Qin Feng. Rapid temperature jump by infrared diode laser irradiation for Patch-Clamp studies. Biophys J, 2009, 96(9): 3611-3619.
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20.	鄭羽, 李靜, 蔡迪, 等. 快電容補償方法對提高神經元細胞動作電位發放精度的影響. 生物醫學工程學雜志, 2014, 31(6): 1191-1194.
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25.	葉燚, 胡剛, 瞿安連. 全自動膜片鉗放大器快電容補償技術改進. 上海生物醫學工程, 2006, 27(2): 98-101.
26.	Kuyucak S, Chung S H. Temperature-dependence of conductivity in electrolyte-solutions and ionic channels of biological-membranes. Biophys Chem, 1994, 52(1): 15-24.
27.	Sakmann B, Neher E. Single-channel recording. New York: Springer US, 1995.
28.	金虎杰, 韓德萬, 王成貴. 液體電阻率與溫度和濃度之間關系的測量. 延邊大學學報(自然科學版), 2003, 29(1): 72-75.
29.	Plaksin M, Shapira E, Kimmel E, et al. Thermal transients excite neurons through universal intramembrane mechanoelectrical effects. Phys Rev X, 2018, 8(1): 2160-3308.
30.	Entwisle B, McMullan S, Bokiniec P, et al. In vitro neuronal depolarization and increased synaptic activity induced by infrared neural stimulation. Biomed Opt Express, 2016, 7(9): 3211-3219.
31.	Schmitt B M, Koepsell H. An improved method for real-time monitoring of membrane capacitance in Xenopus laevis oocytes. Biophys J, 2002, 82(3): 1345-1357.
32.	Farrell B, Do Shope C, Brownell W E. Voltage-dependent capacitance of human embryonic kidney cells. Phys Rev E, 2006, 73(4): 041930.

1. Neher E, Sakmann B. Single-channel currents recorded from membrane of denervated frog muscle-fibers. Nature, 1976, 260(5554): 799-802.
2. Hodgkin A L, Huxley A F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol, 1952, 117(4): 500-544.
3. Hodgkin A L, Huxley A F, Katz B. Measurement of current-voltage relations in the membrane of the giant axon of loligo. J Physiol London, 1952, 116(4): 424-448.
4. Anderson C R, Cull-Candy S G, Miledi R. Potential-dependent transition temperature of ionic channels induced by glutamate in locust muscle. Nature, 1977, 268(5621): 663-665.
5. Paris L, Marc I, Charlot B, et al. Millisecond infrared laser pulses depolarize and elicit action potentials on in-vitro dorsal root ganglion neurons. Biomed Opt Express, 2017, 8(10): 4568-4578.
6. Duke A R, Cayce J M, Malphrus J D, et al. Combined optical and electrical stimulation of neural tissue in vivo. J Biomed Opt, 2009, 14(6): 60501.
7. Jenkins M W, Duke A R, Gu S, et al. Optical pacing of the embryonic heart. Nat Photonics, 2010, 4(9): 623-626.
8. Jiang Bin, Hou Wensheng, Xia Nan, et al. Inhibitory effect of 980-nm laser on neural activity of the rat's cochlear nucleus. Neurophotonics, 2019, 6(3): 035009.
9. Haas A J, Le Page Y, Zhadobov M, et al. Effect of acute millimeter wave exposure on dopamine metabolism of NGF-treated PC12 cells. J Radiat Res, 2017, 58(4): 439-445.
10. De Seze R, Poutriquet C, Gamez C, et al. Repeated exposure to nanosecond high power pulsed microwaves increases cancer incidence in rat. PloS One, 2020, 15(4): e0226858.
11. Haas A J, Le Page Y, Zhadobov M, et al. Effects of 60-GHz millimeter waves on neurite outgrowth in PC12 cells using high-content screening. Neurosci Lett, 2016, 618(4): 58-65.
12. Liu Qiang, Frerck M J, Holman H A, et al. Exciting cell membranes with a blustering heat shock. Biophys J, 2014, 106(8): 1570-1577.
13. Shapiro M G, Homma K, Villarreal S, et al. Infrared light excites cells by changing their electrical capacitance. Nat Commun, 2012, 3: 736.
14. Li Xinyu, Liu Jia, Liang Shanshan, et al. 980-Nm infrared laser modulation of sodium channel kinetics in a neuron cell linearly mediated by photothermal effect. J Biomed Opt, 2014, 19(10): 105002.
15. Shapiro M G, Priest M F, Siegel P H, et al. Thermal mechanisms of millimeter wave stimulation of excitable cells. Biophys J, 2013, 104(12): 2622-2628.
16. Yao Jing, Liu Beiying, Qin Feng. Rapid temperature jump by infrared diode laser irradiation for Patch-Clamp studies. Biophys J, 2009, 96(9): 3611-3619.
17. Bec J M, Albert E S, Marc I, et al. Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons. Lasers Surg Med, 2012, 44(9): 736-745.
18. Wells J, Kao C, Konrad P, et al. Biophysical mechanisms of transient optical stimulation of peripheral nerve. Biophys J, 2007, 93(7): 2567-2580.
19. Moreau D, Lefort C, Pas J, et al. Infrared neural stimulation induces intracellular Ca²⁺ release mediated by phospholipase C. J Biophotonics, 2018, 11(2): e201700020.
20. 鄭羽, 李靜, 蔡迪, 等. 快電容補償方法對提高神經元細胞動作電位發放精度的影響. 生物醫學工程學雜志, 2014, 31(6): 1191-1194.
21. Lothet E H, Shaw K M, Lu Hui, et al. Selective inhibition of small-diameter axons using infrared light. Sci Rep, 2017, 7(1): 3275.
22. Eom K, Byun K M, Jun S B, et al. Theoretical study on gold-nanorod-enhanced near-infrared neural stimulation. Biophys J, 2018, 115(8): 1481-1497.
23. Sigworth F J, Affolter H, Neher E. Design of the EPC-9, a computer-controlled patch-clamp amplifier. 2. Software. J Neurosci Meth, 1995, 56(2): 203-215.
24. Sigworth F J. Design of the EPC-9, a computer-controlled patch-clamp amplifier. 1. Hardware. J Neurosci Meth, 1995, 56(2): 195-202.
25. 葉燚, 胡剛, 瞿安連. 全自動膜片鉗放大器快電容補償技術改進. 上海生物醫學工程, 2006, 27(2): 98-101.
26. Kuyucak S, Chung S H. Temperature-dependence of conductivity in electrolyte-solutions and ionic channels of biological-membranes. Biophys Chem, 1994, 52(1): 15-24.
27. Sakmann B, Neher E. Single-channel recording. New York: Springer US, 1995.
28. 金虎杰, 韓德萬, 王成貴. 液體電阻率與溫度和濃度之間關系的測量. 延邊大學學報(自然科學版), 2003, 29(1): 72-75.
29. Plaksin M, Shapira E, Kimmel E, et al. Thermal transients excite neurons through universal intramembrane mechanoelectrical effects. Phys Rev X, 2018, 8(1): 2160-3308.
30. Entwisle B, McMullan S, Bokiniec P, et al. In vitro neuronal depolarization and increased synaptic activity induced by infrared neural stimulation. Biomed Opt Express, 2016, 7(9): 3211-3219.
31. Schmitt B M, Koepsell H. An improved method for real-time monitoring of membrane capacitance in Xenopus laevis oocytes. Biophys J, 2002, 82(3): 1345-1357.
32. Farrell B, Do Shope C, Brownell W E. Voltage-dependent capacitance of human embryonic kidney cells. Phys Rev E, 2006, 73(4): 041930.

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Study on the temperature characteristics of fast capacitance in patch clamp experiments

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