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Testing an Explicit Method for Multi-compartment Neuron Model Simulation on a GPU

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A Correction to this article was published on 02 March 2022

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Abstract

Large-scale simulation of multi-compartment models is important for understanding the role of morphological structures of individual neurons for information processing in the brain. In a simulation, partial differential equations (PDEs) that describe the dynamics of neurons have to be solved numerically for each time step. To solve PDEs, numerical methods called implicit methods are used for stability. Implicit methods need to solve simultaneous equations, which can make numerical simulation slow on graphics processing units (GPUs) hardware accelerators for parallel computing. To overcome this problem, we investigated the use of explicit methods for multi-compartment model simulation. We applied the Runge–Kutta–Chebyshev (RKC) method to several cerebellar neuron models including Purkinje cells, granule cells, Golgi cells, and inferior olive cells. Next, we implemented a cerebellar cortical model composed of granule cells, Golgi cells, and Purkinje cells, while using different numerical methods for different cell types. Although explicit methods can be unstable against PDEs, using the RKC method showed sufficient stability for most cases, better computational performance than implicit methods on a GPU, and good reproducibility. In the network simulation, choosing the suitable numerical methods for each cell type achieved faster simulation than that used an implicit method solely. Our results suggest that explicit methods are applicable to multi-compartment models and can accelerate computational speed of simulations. Furthermore, to conduct large-scale simulation of multi-compartment models, choosing efficient numerical methods will be more important.

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References

  1. Ananthanarayanan R, Esser SK, Simon HD, Modha DS. The cat is out of the bag: cortical simulations with \(10^{9}\) neurons, \(10^{13}\) synapses. In: Proceedings of the conference on high performance computing networking, storage and analysis. 2009. p. 1–12.

  2. Helias M, Kunkel S, Masumoto G, Igarashi J, Eppler JM, Ishii S, et al. Supercomputers ready for use as discovery machines for neuroscience. Front Neuroinform. 2012;6:26.

    Article  Google Scholar 

  3. Kunkel S, Schmidt M, Eppler JM, Plesser HE, Masumoto G, Igarashi J, et al. Spiking network simulation code for petascale computers. Front Neuroinform. 2014;8:78.

    Article  Google Scholar 

  4. Jordan J, Ippen T, Helias M, Kitayama I, Sato M, Igarashi J, et al. Extremely scalable spiking neuronal network simulation code: from laptops to exascale computers. Front Neuroinform. 2018;12:2.

    Article  Google Scholar 

  5. Jordan J, Helias M, Diesmann M, Kunkel S. Efficient communication in distributed simulations of spiking neuronal networks with gap junctions. Front Neuroinform. 2020;14:12.

    Article  Google Scholar 

  6. Yamaura H, Igarashi J, Yamazaki T. Simulation of a human-scale cerebellar network model on the K computer. Front Neuroinform. 2020;14:16.

    Article  Google Scholar 

  7. Brunel N, Hakim V, Isope P, Nadal J-P, Barbour B. Optimal information storage and the distribution of synaptic weights: perceptron versus Purkinje cell. Neuron. 2004;43(5):745–57.

    Google Scholar 

  8. Zang Y, Dieudonné S, De Schutter E. Voltage-and branch-specific climbing fiber responses in Purkinje cells. Cell Rep. 2018;24(6):1536–49.

    Article  Google Scholar 

  9. Moldwin T, Segev I. Perceptron learning and classification in a modeled cortical pyramidal cell. Front Comput Neurosci. 2020;14.

  10. Traub RD, Contreras D, Cunningham MO, Murray H, LeBeau FE, Roopun A, et al. Single-column thalamocortical network model exhibiting gamma oscillations, sleep spindles, and epileptogenic bursts. J Neurophysiol. 2005;93(4):2194–232.

    Article  Google Scholar 

  11. Traub RD, Middleton SJ, Knöpfel T, Whittington MA. Model of very fast (>75 Hz) network oscillations generated by electrical coupling between the proximal axons of cerebellar Purkinje cells. Eur J Neurosci. 2008;28(8):1603–16.

    Article  Google Scholar 

  12. Izhikevich EM, Edelman GM. Large-scale model of mammalian thalamocortical systems. Proc Natl Acad Sci. 2008;105(9):3593–8.

    Article  Google Scholar 

  13. Markram H, Muller E, Ramaswamy S, Reimann MW, Abdellah M, Sanchez CA, et al. Reconstruction and simulation of neocortical microcircuitry. Cell. 2015;163(2):456–92.

    Article  Google Scholar 

  14. Bezaire MJ, Raikov I, Burk K, Vyas D, Soltesz I. Interneuronal mechanisms of hippocampal theta oscillations in a full-scale model of the rodent CA1 circuit. Elife. 2016;5:e18566.

  15. Sudhakar SK, Hong S, Raikov I, Publio R, Lang C, Close T, et al. Spatiotemporal network coding of physiological mossy fiber inputs by the cerebellar granular layer. PLoS Comput Biol. 2017;13(9):e1005754.

  16. Billeh YN, Cai B, Gratiy SL, Dai K, Iyer R, Gouwens NW, et al. Systematic integration of structural and functional data into multi-scale models of mouse primary visual cortex. Neuron. 2020;106(3):388–403.

    Article  Google Scholar 

  17. Neymotin SA, Daniels DS, Caldwell B, McDougal RA, Carnevale NT, Jas M, et al. Human neocortical neurosolver (HNN), a new software tool for interpreting the cellular and network origin of human MEG/EEG data. Elife. 2020;9:e51214.

  18. Dai K, Gratiy SL, Billeh YN, Xu R, Cai B, Cain N, et al. Brain modeling toolkit: An open source software suite for multiscale modeling of brain circuits. PLoS Comput Biol. 2020;16(11): e1008386.

  19. Hines ML, Carnevale NT. The NEURON simulation environment. Neural Comput. 1997;9(6):1179–209.

    Article  Google Scholar 

  20. Wilson MA, Bhalla US, Uhley JD, Bower JM. GENESIS: a system for simulating neural networks. Adv Neural Inf Proces Syst. 1989;1:485–92.

    Google Scholar 

  21. Kumbhar P, Hines M, Fouriaux J, Ovcharenko A, King J, Delalondre F, et al. CoreNEURON: an optimized compute engine for the NEURON simulator. Front Neuroinform. 2019;13:63.

    Article  Google Scholar 

  22. Abi Akar N, Cumming B, Karakasis V, Küsters A, Klijn W, Peyser A, et al. Arbor – a morphologically-detailed neural network simulation library for contemporary high-performance computing architectures. In 2019 27th Euromicro international conference on parallel, distributed and network-based processing (PDP). IEEE, 2019. p. 274–282.

  23. De Schutter E, Bower JM. An active membrane model of the cerebellar Purkinje cell. I. Simulation of current clamps in slice. J Neurophysiol. 1994;71(1):375–400.

  24. De Schutter E, Bower JM. An active membrane model of the cerebellar Purkinje cell II. Simulation of synaptic responses. J Neurophysiol. 1994);71(1):401–419.

  25. Dover K, Marra C, Solinas S, Popovic M, Subramaniyam S, Zecevic D, et al. FHF-independent conduction of action potentials along the leak-resistant cerebellar granule cell axon. Nat Commun. 2016;7(1):1–11.

    Article  Google Scholar 

  26. Solinas S, Forti L, Cesana E, Mapelli J, De Schutter E, D’Angelo E. Computational reconstruction of pacemaking and intrinsic electroresponsiveness in cerebellar Golgi cells. Front Cell Neurosci. 2007;1:2.

    Google Scholar 

  27. De Gruijl JR, Bazzigaluppi P, de Jeu MT, De Zeeuw CI. Climbing fiber burst size and olivary sub-threshold oscillations in a network setting. PLoS Comput Biol. 2012;8(12): e1002814.

  28. Koch C, Segev I. Methods in neuronal modeling: from ions to networks, 2nd ed. MIT press, 1998.

  29. Solinas S, Nieus T, D’Angelo E. A realistic large-scale model of the cerebellum granular layer predicts circuit spatio-temporal filtering properties. Front Cell Neurosci. 2010;4:12.

  30. Dugué GP, Brunel N, Hakim V, Schwartz E, Chat M, Lévesque M, et al. Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron. 2009;61(1):126–39.

    Article  Google Scholar 

  31. Vervaeke K, Lőrincz A, Gleeson P, Farinella M, Nusser Z, Silver RA. Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron. 2010;67(3):435–51.

    Article  Google Scholar 

  32. Vervaeke K, Lőrincz A, Nusser Z, Silver RA. Gap junctions compensate for sublinear dendritic integration in an inhibitory network. Science. 2012;335(6076):1624–8.

    Article  Google Scholar 

  33. Shin S-L, De Schutter E. Dynamic synchronization of Purkinje cell simple spikes. J Neurophysiol. 2006;96(6):3485–91.

    Article  Google Scholar 

  34. Wise AK, Cerminara NL, Marple-Horvat DE, Apps R. Mechanisms of synchronous activity in cerebellar Purkinje cells. J Physiol. 2010;588(13):2373–90.

    Article  Google Scholar 

  35. Verwer JG, Hundsdorfer WH, Sommeijer BP. Convergence properties of the Runge-Kutta-Chebyshev method. Numer Math. 1990;57(1):157–78.

    Article  MathSciNet  MATH  Google Scholar 

  36. Verwer JG. Explicit Runge-Kutta methods for parabolic partial differential equations. Appl Numer Math. 1996;22(1–3):359–79.

    Article  MathSciNet  MATH  Google Scholar 

  37. Van der Houwen P. The development of Runge-Kutta methods for partial differential equations. Appl Numer Math. 1996;20(3):261–72.

    Article  MathSciNet  MATH  Google Scholar 

  38. Sommeijer BP, Shampine LF, Verwer JG. RKC: An explicit solver for parabolic PDEs. J Comput Appl Math. 1998;88(2):315–26.

    Article  MathSciNet  MATH  Google Scholar 

  39. Verwer JG, Sommeijer BP, Hundsdorfer W. RKC time-stepping for advection-diffusion-reaction problems. J Comput Phys. 2004;201(1):61–79.

    Article  MathSciNet  MATH  Google Scholar 

  40. NVIDIA. CUDA C Programming Guide. https://docs.nvidia.com/cuda/pdf/CUDA_C_Programming_Guide.pdf, 2021. Accessed 24 March 2021.

  41. NVIDIA. CUBLAS Library. https://docs.nvidia.com/cuda/pdf/CUBLAS_Library.pdf, 2021. Accessed 24 March 2021.

  42. Hines M. Efficient computation of branched nerve equations. Int J Biomed Comput. 1984;15(1):69–76.

    Article  Google Scholar 

  43. NVIDIA. CUDA Profiler User’s Guide. https://docs.nvidia.com/cuda/profiler-users-guide/index.html#nvprof-overview, 2021. Accessed 16 July 2021.

  44. NVIDIA. CUDA C++ Best Practices Guide. https://docs.nvidia.com/cuda/cuda-c-best-practices-guide/index.html, 2021. Accessed 16 July 2021.

  45. Pernelle G, Nicola W, Clopath C. Gap junction plasticity as a mechanism to regulate network-wide oscillations. PLoS Comput Biol. 2018;14(3):e1006025.

  46. Bennett MV, Zukin RS. Electrical coupling and neuronal synchronization in the mammalian brain. Neuron. 2004;41(4):495–511.

    Article  Google Scholar 

  47. Middleton SJ, Racca C, Cunningham MO, Traub RD, Monyer H, Knöpfel T, et al. High-frequency network oscillations in cerebellar cortex. Neuron. 2008;58(5):763–74.

    Article  Google Scholar 

  48. Blenkinsop TA, Lang EJ. Block of inferior olive gap junctional coupling decreases purkinje cell complex spike synchrony and rhythmicity. J Neurosci. 2006;26(6):1739–48.

    Article  Google Scholar 

  49. de Solages C, Szapiro G, Brunel N, Hakim V, Isope P, Buisseret P, et al. High-frequency organization and synchrony of activity in the purkinje cell layer of the cerebellum. Neuron. 2008;58(5):775–88.

    Article  Google Scholar 

  50. Han K-S, Guo C, Chen CH, Witter L, Osorno T, Regehr WG. Ephaptic coupling promotes synchronous firing of cerebellar Purkinje cells. Neuron. 2018;100(3):564–78.

    Article  Google Scholar 

  51. Ishikawa T, Shimuta M, Häusser M. Multimodal sensory integration in single cerebellar granule cells in vivo. Elife. 2015;4:e12916.

  52. Majoral D, Zemmar A, Vicente R. A model for time interval learning in the Purkinje cell. PLoS Comput Biol. 2020;16(2):e1007601.

  53. Karimov AI, Butusov DN, Tutueva AV. Adaptive explicit-implicit switching solver for stiff ODEs. In: 2017 IEEE Conference of Russian Young Researchers in Electrical and Electronic Engineering (EIConRus). IEEE; 2017. p. 440–444.

  54. Sofroniou M, Spaletta G. Extrapolation methods in mathematica. JNAIAM J Numer Anal Indust Appl Math. 2008;(3):105–121.

  55. Niemeyer KE, Sung C-J. Accelerating moderately stiff chemical kinetics in reactive-flow simulations using GPUs. J Comput Phys. 2014;256:854–71.

    Article  MathSciNet  MATH  Google Scholar 

  56. Brette R, Rudolph M, Carnevale T, Hines M, Beeman D, Bower JM, et al. Simulation of networks of spiking neurons: a review of tools and strategies. J Comput Neurosci. 2007;23(3):349–98.

    Article  MathSciNet  Google Scholar 

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Acknowledgements

We would like to thank Messrs. Tsukasa Tsuyuki and Yuki Yamamoto for preliminary investigation of multi-compartment models. We also thank Professors Junichiro Makino in Kobe University and Toshikazu Ebisuzaki in RIKEN for their comments on the use of explicit methods for diffusion equations. This study was supported by MEXT/JSPS Kakenhi Grant Numbers 17H06310 and 20K06850, Japanese Neural Network Society 30th Anniversary Fund, and an intramural fund of the University of Electro-Communications.

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Correspondence to Tadashi Yamazaki.

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Kobayashi, T., Kuriyama, R. & Yamazaki, T. Testing an Explicit Method for Multi-compartment Neuron Model Simulation on a GPU. Cogn Comput 15, 1118–1131 (2023). https://doi.org/10.1007/s12559-021-09942-6

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