Effect of Optogenetic Stimulation Parameters on Firing Rate of Basal Ganglia Neurons in Parkinsonian State BG and RT Networks
-
Nazlar Ghasemzadeh
,
Fereidoun Nowshiravan Rahatabad
,
Siamak Haghipour
,
Shabnam Andalibi Miandoab
,
Keivan Maghooli
Abstract
Purpose: Parkinson's disease is a neurodegenerative disorder that affects the basal ganglia of the brain, which plays an important role in movement. Basal Ganglia-Thalamic network model including Subthalamic nucleus, Globus Pallidus externa, Globus Pallidus interna and Thalamus neurons. Optogenetics is a combination of optical and genetic tools used to stimulate basal ganglia neurons by light-sensitive ion channels (opsins) to eliminate the pathological effects of Parkinson's disease.
Materials and Methods: To analyze the effect of optogenetic stimulation on Parkinsonian nervous systems, two complete models of BG and RT (including STN, GPe, Gpi, and TH neurons) have been selected and developed for Parkinson’s disease and to apply three and four-state optogenetic stimulation. For this purpose, ChETA, ChRwt, and NpHR opsins have been selected in three-state and four-state stimulations and different stimulation conditions according to different parameters in both models have been investigated.
Results: To evaluate the performance of two models for each gene in three- and four-state stimulation conditions with different values of basic parameters, the value of error index is calculated and stimulation conditions that created an error index equal to zero have been introduced as optimal conditions. Based on the results, frequencies of 20 and 200 Hz in the four-state ChRwt model and frequency of 80 Hz in the three-state ChETA model have been introduced as optimal genes, frequencies, and models. To verify the developed model, the obtained results have been compared with the results of experimental studies.
Conclusion: In optimal conditions, STN provides excitatory input and GPe provide appropriate inhibitory input to GPi, and GPi can provide appropriate inhibitory input to TH, and as a result, its function improves and pathological effects of Parkinson's disease disappear. The response of GPe neurons is consistent with the experimental results and the response of other neurons is also similar to the response of GPe neurons.
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22- Georg Nagel et al., "Channelrhodopsin-1: a light-gated proton channel in green algae." Science, Vol. 296 (No. 5577), pp. 2395-98, (2002).
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24- Caspar Glock, Jatin Nagpal, and Alexander Gottschalk, "Microbial rhodopsin optogenetic tools: application for analyses of synaptic transmission and of neuronal network activity in behavior." C. elegans: Methods and Applications, pp. 87-103, (2015).
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26- Feng Zhang, Li-Ping Wang, Edward S Boyden, and Karl Deisseroth, "Channelrhodopsin-2 and optical control of excitable cells." Nature methods, Vol. 3 (No. 10), pp. 785-92, (2006).
27- Roxana A Stefanescu, RG Shivakeshavan, Pramod P Khargonekar, and Sachin S Talathi, "Computational modeling of channelrhodopsin-2 photocurrent characteristics in relation to neural signaling." Bulletin of mathematical biology, Vol. 75pp. 2208-40, (2013).
28- Rosa Q So, Alexander R Kent, and Warren M Grill, "Relative contributions of local cell and passing fiber activation and silencing to changes in thalamic fidelity during deep brain stimulation and lesioning: a computational modeling study." Journal of computational neuroscience, Vol. 32 (No. 3), pp. 499-519, (2012).
29- Shivakeshavan Ratnadurai-Giridharan, Chung C Cheung, and Leonid L Rubchinsky, "Effects of electrical and optogenetic deep brain stimulation on synchronized oscillatory activity in parkinsonian basal ganglia." IEEE Transactions on Neural Systems and Rehabilitation Engineering, Vol. 25 (No. 11), pp. 2188-95, (2017).
30- Nazlar Ghasemzadeh, Fereidoun Nowshiravan Rahatabad, Siamak Haghipour, Shabnam Andalibi Miandoab, and Keivan Maghooli, "Controlling pathological activity of Parkinson basal ganglia based on excitation and inhibition optogenetic models and monophasic and biphasic electrical stimulations." Journal of Biosciences, Vol. 48 (No. 4), p. 40, (2023).
31- Terman, D., et al., Activity patterns in a model for the subthalamopallidal network of the basal ganglia. Journal of Neuroscience, 2002. 22(7): p. 2963-2976.
32- Rubin, J.E. and D. Terman, High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. Journal of computational neuroscience, 2004. 16: p. 211-235.
33- ALFRED Meyer, "The concept of a sensorimotor cortex: its early history, with especial emphasis on two early experimental contributions by W. Bechterew." Brain: a journal of neurology, Vol. 101 (No. 4), pp. 673-85, (1978).
34- TJ Torrico and S Munakomi, "Neuroanatomy, Thalamus.[Updated 2021 Jul 31]." StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing, Vol. 1(2022).
35- Peter Hegemann, Sabine Ehlenbeck, and Dietrich Gradmann, "Multiple photocycles of channelrhodopsin." Biophysical journal, Vol. 89 (No. 6), pp. 3911-18, (2005).
36- Konstantin Nikolic, Patrick Degenaar, and Chris Toumazou, "Modeling and engineering aspects of channelrhodopsin2 system for neural photostimulation." in 2006 International Conference of the IEEE Engineering in Medicine and Biology Society, (2006): IEEE, pp. 1626-29.
37- Jessica A Cardin et al., "Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2." Nature protocols, Vol. 5 (No. 2), pp. 247-54, (2010).
38- Zahra Noraepour, Mohammad Ismail Zibaii, Leila Dargahi, and hamid Latifi, "Modeling and study of Rhodopsin proteins responses to laser light irradiance in ultrafast optogenetic control." (in eng), Accepted and Presented Articles of OPSI Conferences, Research Vol. 24 (No. 0), pp. 569-72, (2018).
39- Viviana Gradinaru, Kimberly R Thompson, and Karl Deisseroth, "eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications." Brain cell biology, Vol. 36pp. 129-39, (2008).
40- Lisa A Gunaydin, Ofer Yizhar, André Berndt, Vikaas S Sohal, Karl Deisseroth, and Peter Hegemann, "Ultrafast optogenetic control." Nature neuroscience, Vol. 13 (No. 3), pp. 387-92, (2010).
41- André Berndt et al., "High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels." Proceedings of the National Academy of Sciences, Vol. 108 (No. 18), pp. 7595-600, (2011).
42- Xiao-Jing Wang and György Buzsáki, "Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model." Journal of Neuroscience, Vol. 16 (No. 20), pp. 6402-13, (1996).
43- Denggui Fan, Zhihui Wang, and Qingyun Wang, "Optimal control of directional deep brain stimulation in the parkinsonian neuronal network." Communications in Nonlinear Science and Numerical Simulation, Vol. 36pp. 219-37, (2016).
2- Elham Samadi, Hessam Ahmadi, and Fereidoun Nowshiravan Rahatabad, "Analysis of Hand Tremor in Parkinson’s Disease: Frequency Domain Approach." Frontiers in Biomedical Technologies, Vol. 7 (No. 2), pp. 105-11, (2020).
3- Krystal L Parker, Youngcho Kim, Stephanie L Alberico, Eric B Emmons, and Nandakumar S Narayanan, "Optogenetic approaches to evaluate striatal function in animal models of Parkinson disease." Dialogues in clinical neuroscience, (2022).
4- R Prashanth and Sumantra Dutta Roy, "Early detection of Parkinson’s disease through patient questionnaire and predictive modelling." International journal of medical informatics, Vol. 119pp. 75-87, (2018).
5- Vasilis Ntziachristos, "Fluorescence molecular imaging." Annu. Rev. Biomed. Eng., Vol. 8pp. 1-33, (2006).
6- Ralph Weissleder and Vasilis Ntziachristos, "Shedding light onto live molecular targets." Nature medicine, Vol. 9 (No. 1), pp. 123-28, (2003).
7- Claudio Vinegoni, Daniel Razansky, Jose-Luiz Figueiredo, Matthias Nahrendorf, Vasilis Ntziachristos, and Ralph Weissleder, "Normalized Born ratio for fluorescence optical projection tomography." Optics letters, Vol. 34 (No. 3), pp. 319-21, (2009).
8- Mark G Van Vledder et al., "The effect of steatosis on echogenicity of colorectal liver metastases on intraoperative ultrasonography." Archives of surgery, Vol. 145 (No. 7), pp. 661-67, (2010).
9- Osamu Ukimura, Koji Okihara, Kazumi Kamoi, Yoshio Naya, Atsushi Ochiai, and Tsuneharu Miki, "Intraoperative ultrasonography in an era of minimally invasive urology." International journal of urology, Vol. 15 (No. 8), pp. 673-80, (2008).
10- Dushyant V Sahani et al., "Intraoperative US in patients undergoing surgery for liver neoplasms: comparison with MR imaging." Radiology, Vol. 232 (No. 3), pp. 810-14, (2004).
11- Shabnam Andalibi Miandoab and Robabeh Talebzadeh, "Ultra-sensitive and selective 2D hybrid highly doped semiconductor-graphene biosensor based on SPR and SEIRA effects in the wide range of infrared spectral." Optical Materials, Vol. 129p. 112572, (2022).
12- Amir Asadzade and Shabnam Andalibi Miandoab, "Design and simulation of 3D perovskite solar cells based on titanium dioxide nanowires to achieve high-efficiency." Solar Energy, Vol. 228pp. 550-61, (2021).
13- Katyani R and Andalibi Miandoab S, "Enhance efficiency in flat and nano roughness surface perovskite solar cells with the use of index near zero materials filter." Optical and Quantum Electronics., Vol. 53 (No. 9), (2021).
14- Silvia Skripenova and Lester J Layfield, "Initial margin status for invasive ductal carcinoma of the breast and subsequent identification of carcinoma in reexcision specimens." Archives of pathology & laboratory medicine, Vol. 134 (No. 1), pp. 109-14, (2010).
15- Charlotte Holm, M Mayr, E Höfter, A Becker, UJ Pfeiffer, and W Mühlbauer, "Intraoperative evaluation of skin-flap viability using laser-induced fluorescence of indocyanine green." British journal of plastic surgery, Vol. 55 (No. 8), pp. 635-44, (2002).
16- Alexander Erofeev et al., "Light stimulation parameters determine neuron dynamic characteristics." Applied Sciences, Vol. 9 (No. 18), p. 3673, (2019).
17- Ruben Schoeters, Thomas Tarnaud, Wout Joseph, Luc Martens, Robrecht Raedt, and Emmeric Tanghe, "Comparison between direct electrical and optogenetic subthalamic nucleus stimulation." in 2018 EMF-Med 1st World Conference on Biomedical Applications of Electromagnetic Fields (EMF-Med), (2018): IEEE, pp. 1-2.
18- Karl Deisseroth, Guoping Feng, Ania K Majewska, Gero Miesenböck, Alice Ting, and Mark J Schnitzer, "Next-generation optical technologies for illuminating genetically targeted brain circuits." Journal of Neuroscience, Vol. 26 (No. 41), pp. 10380-86, (2006).
19- Honghui Zhang, Ying Yu, Zichen Deng, and Qingyun Wang, "Activity pattern analysis of the subthalamopallidal network under ChannelRhodopsin-2 and Halorhodopsin photocurrent control." Chaos, Solitons & Fractals, Vol. 138p. 109963, (2020).
20- Allison E Girasole et al., "A subpopulation of striatal neurons mediates levodopa-induced dyskinesia." Neuron, Vol. 97 (No. 4), pp. 787-95. e6, (2018).
21- Jan Tønnesen, "Optogenetic cell control in experimental models of neurological disorders." Behavioural brain research, Vol. 255pp. 35-43, (2013).
22- Georg Nagel et al., "Channelrhodopsin-1: a light-gated proton channel in green algae." Science, Vol. 296 (No. 5577), pp. 2395-98, (2002).
23- Georg Nagel et al., "Channelrhodopsin-2, a directly light-gated cation-selective membrane channel." Proceedings of the National Academy of Sciences, Vol. 100 (No. 24), pp. 13940-45, (2003).
24- Caspar Glock, Jatin Nagpal, and Alexander Gottschalk, "Microbial rhodopsin optogenetic tools: application for analyses of synaptic transmission and of neuronal network activity in behavior." C. elegans: Methods and Applications, pp. 87-103, (2015).
25- Nir Grossman, Konstantin Nikolic, Christofer Toumazou, and Patrick Degenaar, "Modeling study of the light stimulation of a neuron cell with channelrhodopsin-2 mutants." IEEE Transactions on Biomedical Engineering, Vol. 58 (No. 6), pp. 1742-51, (2011).
26- Feng Zhang, Li-Ping Wang, Edward S Boyden, and Karl Deisseroth, "Channelrhodopsin-2 and optical control of excitable cells." Nature methods, Vol. 3 (No. 10), pp. 785-92, (2006).
27- Roxana A Stefanescu, RG Shivakeshavan, Pramod P Khargonekar, and Sachin S Talathi, "Computational modeling of channelrhodopsin-2 photocurrent characteristics in relation to neural signaling." Bulletin of mathematical biology, Vol. 75pp. 2208-40, (2013).
28- Rosa Q So, Alexander R Kent, and Warren M Grill, "Relative contributions of local cell and passing fiber activation and silencing to changes in thalamic fidelity during deep brain stimulation and lesioning: a computational modeling study." Journal of computational neuroscience, Vol. 32 (No. 3), pp. 499-519, (2012).
29- Shivakeshavan Ratnadurai-Giridharan, Chung C Cheung, and Leonid L Rubchinsky, "Effects of electrical and optogenetic deep brain stimulation on synchronized oscillatory activity in parkinsonian basal ganglia." IEEE Transactions on Neural Systems and Rehabilitation Engineering, Vol. 25 (No. 11), pp. 2188-95, (2017).
30- Nazlar Ghasemzadeh, Fereidoun Nowshiravan Rahatabad, Siamak Haghipour, Shabnam Andalibi Miandoab, and Keivan Maghooli, "Controlling pathological activity of Parkinson basal ganglia based on excitation and inhibition optogenetic models and monophasic and biphasic electrical stimulations." Journal of Biosciences, Vol. 48 (No. 4), p. 40, (2023).
31- Terman, D., et al., Activity patterns in a model for the subthalamopallidal network of the basal ganglia. Journal of Neuroscience, 2002. 22(7): p. 2963-2976.
32- Rubin, J.E. and D. Terman, High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. Journal of computational neuroscience, 2004. 16: p. 211-235.
33- ALFRED Meyer, "The concept of a sensorimotor cortex: its early history, with especial emphasis on two early experimental contributions by W. Bechterew." Brain: a journal of neurology, Vol. 101 (No. 4), pp. 673-85, (1978).
34- TJ Torrico and S Munakomi, "Neuroanatomy, Thalamus.[Updated 2021 Jul 31]." StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing, Vol. 1(2022).
35- Peter Hegemann, Sabine Ehlenbeck, and Dietrich Gradmann, "Multiple photocycles of channelrhodopsin." Biophysical journal, Vol. 89 (No. 6), pp. 3911-18, (2005).
36- Konstantin Nikolic, Patrick Degenaar, and Chris Toumazou, "Modeling and engineering aspects of channelrhodopsin2 system for neural photostimulation." in 2006 International Conference of the IEEE Engineering in Medicine and Biology Society, (2006): IEEE, pp. 1626-29.
37- Jessica A Cardin et al., "Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2." Nature protocols, Vol. 5 (No. 2), pp. 247-54, (2010).
38- Zahra Noraepour, Mohammad Ismail Zibaii, Leila Dargahi, and hamid Latifi, "Modeling and study of Rhodopsin proteins responses to laser light irradiance in ultrafast optogenetic control." (in eng), Accepted and Presented Articles of OPSI Conferences, Research Vol. 24 (No. 0), pp. 569-72, (2018).
39- Viviana Gradinaru, Kimberly R Thompson, and Karl Deisseroth, "eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications." Brain cell biology, Vol. 36pp. 129-39, (2008).
40- Lisa A Gunaydin, Ofer Yizhar, André Berndt, Vikaas S Sohal, Karl Deisseroth, and Peter Hegemann, "Ultrafast optogenetic control." Nature neuroscience, Vol. 13 (No. 3), pp. 387-92, (2010).
41- André Berndt et al., "High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels." Proceedings of the National Academy of Sciences, Vol. 108 (No. 18), pp. 7595-600, (2011).
42- Xiao-Jing Wang and György Buzsáki, "Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model." Journal of Neuroscience, Vol. 16 (No. 20), pp. 6402-13, (1996).
43- Denggui Fan, Zhihui Wang, and Qingyun Wang, "Optimal control of directional deep brain stimulation in the parkinsonian neuronal network." Communications in Nonlinear Science and Numerical Simulation, Vol. 36pp. 219-37, (2016).
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| Issue | Vol 11 No 3 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/fbt.v11i3.15883 | |
| Keywords | ||
| Parkinson’s Disease Optogenetic Stimulation Basal Ganglia Network Model Rubin-Terman Network Model | ||
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How to Cite
1.
Ghasemzadeh N, Nowshiravan Rahatabad F, Haghipour S, Andalibi Miandoab S, Maghooli K. Effect of Optogenetic Stimulation Parameters on Firing Rate of Basal Ganglia Neurons in Parkinsonian State BG and RT Networks. Frontiers Biomed Technol. 2024;11(3):389-414.
