Simulation of voltage-gated ion channels behavior during infrared neural inhibition (INI)
محورهای موضوعی : Interaction of Light with Tissue and Cells
Mohamamd Ali Ansari
1
(Velenjak)
Hassan Tajarehnejad Abdollahi
2
(Laser and Plasma Research Institute, Shahid Beheshti University, Tehran, Iran, 1983969411)
کلید واژه: infrared, Ion channel, Action potential, Neural block,
چکیده مقاله :
Infrared (IR) radiation is a non-invasive method to reduce neural responses, while its mechanism is still unclear. Here, using the modified Hodgkin-Huxley model, the effects of IR light on the parameters participating in the action potential (AP) blocking are investigated to study the mechanism of infrared neural inhibition (INI). Considering the temperature dependence neural model, the voltage membrane changing, ion currents variation and ion channels activation/inactivation gates behavior under IR pulses are studied. The results show that IR pulses can successfully block APs and confirm that potassium ion currents have an influential role in suppressing APs. Moreover, it is shown that infrared light during the suppression of AP has little effect on increasing the sodium ion currents. However, it seems that sodium ion channel gates play an effective role during INI. It is observed that infrared light increases the rate of opening and closing of activation/inactivation gates of ion channels. This study also presents why the suppression of action potentials continues after the end of the IR pulse. It seems this is related to the incomplete refractory period of AP, which is probably due to the disturbance in the reopening of the sodium channel inactivation gate (h-gate). The current report helps to improve the IR laser medical applications for reducing nerve pain.
[1] M. H. Pitcher, M. Von Korff, M. C. Bushnell, and L. Porter, “Prevalence and Profile of High-Impact Chronic Pain in the United States,” J. Pain, vol. 20, no. 2, pp. 146–160, 2019.
[2] K. Yu, X. Niu, and B. He, “Neuromodulation Management of Chronic Neuropathic Pain in the Central Nervous System,” Adv. Funct. Mater, vol. 30, no. 37, pp. 1908999 (1-36), 2020.
[3] S. R. Tsai and M. R. Hamblin, “Biological effects and medical applications of infrared radiation,” Journal of Photochemistry and Photobiology B: Biology, vol. 170. Elsevier B.V, pp. 197–207, 2017.
[4] E.H. Lothet, K.M. Shaw, H. Lu, J. Zhuo, Y.T. Wang, and S. Gu “Selective inhibition of small-diameter axons using infrared light,” Sci. Rep. vol. 7, no. 1, pp. 1–8, 2017.
[5] Q. Xia and T. Nyberg, “Inhibition of cortical neural networks using infrared laser,” J. Biophotonics, vol. 12, no. 7, pp. e201800403, 2019.
[6] A. J. Walsh, G. P. Tolstykh, S. Martens, B. L. Ibey, and H. T. Beier, “Action potential block in neurons by infrared light,” Neurophotonics, vol. 3, no. 4, pp. 040501 (1-5), 2016.
[7] J. M. Cayce, R. M. Friedman, E. D. Jansen, A. Mahavaden-Jansen, and A. W. Roe, “Pulsed infrared light alters neural activity in rat somatosensory cortex in vivo,” Neuroimage, vol. 57, no. 1, pp. 155–166, 2011.
[8] M. G. Shapiro, K. Homma, S. Villarreal, C. P. Richter, and F. Bezanilla, “Infrared light excites cells by changing their electrical capacitance,” Nat. Commun. vol. 3, no. 1, pp. 1–11, 2012.
[9] A. R. Duke, M. W. Jenkins, H. Lu, J. M. McManus, H. J. Chiel, and E. D. Jansen, “Transient and selective suppression of neural activity with infrared light,” Sci. Rep. vol. 3, no. 1, pp. 1–8, 2013.
[10] Z. Mou, I. F. Triantis, V. M. Woods, C. Toumazou, and K. Nikolic, “A simulation study of the combined thermoelectric extracellular stimulation of the sciatic nerve of the xenopus laevis: The localized transient heat block,” IEEE Trans. Biomed. Eng. vol. 59, pp. 1758–1769, 2012.
[11] M. H. Niemz, Light Acting on Matter, in Laser-Tissue Interactions, Springer International Publishing, 2019.
[12] A. J. Saubermann and V. L. Scheid, “Elemental Composition and Water Content of Neuron and Glial Cells in the Central Nervous System of the North American Medicinal Leech (Macrobdella decora),” J. Neurochem. vol. 44, no. 3, pp. 825–834, 1985.
[13] Q. Xia and T. Nyberg, “Photothermal inhibition of cortex neurons activity by infrared lasXia Q, Nyberg T (2019) Photothermal inhibition of cortex neurons activity by infrared laser. In: IFMBE Proceedings. Springer Verlag, pp 99–104er,” in IFMBE Proceedings, vol. 68, no. 3, pp. 99–104, 2019.
[14] A. L. Hodgkin and A. F. Huxley, “A quantitative description of membrane current and its application to conduction and excitation in nerve,” J. Physiol. vol. 117, no. 4, pp. 500–544, 1952.
[15] S. Fribance, J. Wang, J. R. Roppolo, W. C. de Groat, and C. Tai, “Axonal model for temperature stimulation,” J. Comput. Neurosci. vol. 41, no. 2, pp. 185–192, 2016.
[16] M. A. Ansari and V. V. Tuchin, “Infrared neurostimulation of earthworm: from modeling to experiment,” Opt. Eng. vol. 59, no. 06, pp.1-11, 2020.
[17] Á. Csaba Horváth, S. Borbély, Ö. Csanád Boros, L. Komáromi, P. Koppa, P. Barthó, and Z. Fekete “Infrared neural stimulation and inhibition using an implantable silicon photonic microdevice,” Microsystems Nanoeng. vol. 6, pp. 1–12, 2020.
[18] M. L. Hines and N. T. Carnevale, “The NEURON Simulation Environment,” Neural Computation, vol. 9, pp. 1179–1209, 1997.
[19] H. Richard Leuchtag, “Fit of the dielectric anomaly of squid axon membrane near heat-block temperature to the ferroelectric Curie-Weiss law,” Biophys. Chem. vol. 53, no. 3, pp. 197–205, 1995.
[20] A. L. Hodgkin and B. Katz, “The effect of temperature on the electrical activity of the giant axon of the squid,” J. Physiol. vol. 109, no. 1–2, pp. 240–249, 1949.
[21] Q. Liu, M. J. Frerck, H. A. Holman, E. M. Jorgensen, and R. D. Rabbitt, “Exciting cell membranes with a blustering heat shock,” Biophys. J. vol. 106, no. 8, pp. 1570–1577, 2014.
[22] Y. Xu, R. Wang, S. Ma, L. Zhou, Y. R. Shen, and C. Tian, “Theoretical analysis and simulation of pulsed laser heating at interface,” J. Appl. Phys. vol. 123, no. 2, pp. 025301, 2018.
[23] G. Arias-Gil, F. W. Ohl, K. Takagaki, and M. T. Lippert, “Measurement, modeling, and prediction of temperature rise due to optogenetic brain stimulation,” Neurophotonics, vol. 3, no. 4, pp. 045007 (1-12), 2016.
[24] D. Shepardson, “Algorithms for inverting Hodgkin-Huxley type neuron models,” Georgia Institute of Technology, 2009. Accessed: May 01, 2021. [Online]. Available: http://hdl.handle.net/1853/31686
[25] W. Heitler, “The Hodgkin-Huxley Model for the Generation of Action Potentials,” Feb. 2020. https://www.st-andrews.ac.uk/~wjh/hh_model_intro/ (accessed May 01, 2021).
[26] X. Zhu, J.-W. Lin, and M. Y. Sander, “Infrared inhibition and waveform modulation of action potentials in the crayfish motor axon,” Biomed. Opt. Express, vol. 10, vol. 6580–6594, 2019.
[27] M. Y. Sander, J.-W. Lin, and X. Zhu, “Infrared block of Na+ and Ca2+ spikes in in crayfish neuromuscular junction,” in Optogenetics and Optical Manipulation , vol. 10866, pp. 108660E (1-8), 2019.
[28] M. Ganguly, J. B. Ford, J. Zhuo, M. T. McPheeters, M. W. Jenkins, H. J. Chiel, E. D. Jansen, “Voltage-gated potassium channels are critical for infrared inhibition of action potentials: an experimental study,” Neurophotonics, vol. 6, no. 04, p. 1, Oct. 2019.
[29] X. Liu, Z. Qiao, Y. Chai, Z. Zhu, K. Wu, W. Ji, D. Li, Y. Xiao, L. Mao, Ch. Chang, Q. Wen, B. Song, and Y. Shui, “Nonthermal and reversible control of neuronal signaling and behavior by midinfrared stimulation,” Proc. Natl. Acad. Sci. U. S. A. vol. 118, no. 10, pp. e2015685118 (1-9), 2021.
[30] M. Ganguly, M. W. Jenkins, E. D. Jansen, and H. J. Chiel, “Thermal block of action potentials is primarily due to voltage-dependent potassium currents: A modeling study,” J. Neural Eng. vol. 16, no. 3, pp. 036020, 2019.
[31] Z. Feng, Y. Yu, Z. Guo, J. Cao, and D. M. Durand, “High frequency stimulation extends the refractory period and generates axonal block in the rat hippocampus,” Brain Stimul. vol. 7, no. 5, pp. 680–689, 2014.
[32] Y. Xu, M. Magnuson, A. Agarwal, X. Tan, and C. P. Richter, “Infrared neural stimulation at different wavelengths and pulse shapes,” Prog. Biophys. Mol. Biol. 2021.
