Journal of Computational Neuroscience

, Volume 42, Issue 2, pp 177–185 | Cite as

Propagation and synchronization of reverberatory bursts in developing cultured networks

  • Chih-Hsu Huang
  • Yu-Ting Huang
  • Chun-Chung Chen
  • C. K. Chan
Article
  • 360 Downloads

Abstract

Developing networks of neural systems can exhibit spontaneous, synchronous activities called neural bursts, which can be important in the organization of functional neural circuits. Before the network matures, the activity level of a burst can reverberate in repeated rise-and-falls in periods of hundreds of milliseconds following an initial wave-like propagation of spiking activity, while the burst itself lasts for seconds. To investigate the spatiotemporal structure of the reverberatory bursts, we culture dissociated, rat cortical neurons on a high-density multi-electrode array to record the dynamics of neural activity over the growth and maturation of the network. We find the synchrony of the spiking significantly reduced following the initial wave and the activities become broadly distributed spatially. The synchrony recovers as the system reverberates until the end of the burst. Using a propagation model we infer the spreading speed of the spiking activity, which increases as the culture ages. We perform computer simulations of the system using a physiological model of spiking networks in two spatial dimensions and find the parameters that reproduce the observed resynchronization of spiking in the bursts. An analysis of the simulated dynamics suggests that the depletion of synaptic resources causes the resynchronization. The spatial propagation dynamics of the simulations match well with observations over the course of a burst and point to an interplay of the synaptic efficacy and the noisy neural self-activation in producing the morphology of the bursts.

Keywords

Bursting Reverberation Synchronization Cultured network Simulation 

Supplementary material

10827_2016_634_MOESM1_ESM.zip (6.6 mb)
(ZIP 6.56 MB)

References

  1. Bermudez Contreras, E.J., Schjetnan, A.G.P., Muhammad, A., Bartho, P., McNaughton, B.L., Kolb, B., Gruber, A.J., & Luczak, A. (2013). Formation and reverberation of sequential neural activity patterns evoked by sensory stimulation are enhanced during cortical desynchronization. Neuron, 79(3), 555–566.CrossRefPubMedGoogle Scholar
  2. Bi, G.Q., & Poo, MM (2001). Synaptic modification by correlated activity: Hebb’s postulate revisited. Annual Review of Neuroscience, 24(1), 139–166.CrossRefPubMedGoogle Scholar
  3. Blankenship, A.G., & Feller, M.B. (2010). Mechanisms underlying spontaneous patterned activity in developing neural circuits. Nature Reviews Neuroscience, 11(1), 18–29.CrossRefPubMedGoogle Scholar
  4. Chen, C.C. (2016a). chnchg/cst: common simulation tools. Zenodo. doi:10.5281/zenodo.163650.
  5. Chen, C.C. (2016b). chnchg/measim: simulation of two-dimensional cultured neuronal network. Zenodo. doi:10.5281/zenodo.166691.
  6. Chiappalone, M., Bove, M., Vato, A., Tedesco, M., & Martinoia, S. (2006). Dissociated cortical networks show spontaneously correlated activity patterns during in vitro development. Brain Research, 1093(1), 41–53.CrossRefPubMedGoogle Scholar
  7. Cohen, D., & Segal, M. (2011). Network bursts in hippocampal microcultures are terminated by exhaustion of vesicle pools. Journal of Neurophysiology, 106(5), 2314–2321.CrossRefPubMedGoogle Scholar
  8. Compte, A. (2006). Computational and in vitro studies of persistent activity: edging towards cellular and synaptic mechanisms of working memory. Neuroscience, 139(1), 135–151.CrossRefPubMedGoogle Scholar
  9. Cossart, R. (2014). Operational hub cells: a morpho-physiologically diverse class of GABAergic neurons united by a common function. Current Opinion in Neurobiology, 26, 51–56.CrossRefPubMedGoogle Scholar
  10. Crair, M.C. (1999). Neuronal activity during development: permissive or instructive? Current Opinion in Neurobiology, 9(1), 88–93.CrossRefPubMedGoogle Scholar
  11. Czarnecki, A., Tscherter, A., & Streit, J. (2012). Network activity and spike discharge oscillations in cortical slice cultures from neonatal rat. European Journal of Neuroscience, 35(3), 375–388.CrossRefPubMedGoogle Scholar
  12. Dranias, M.R., Ju, H., Rajaram, E., & VanDongen, A.M.J. (2013). Short-Term memory in networks of dissociated cortical neurons. The Journal of Neuroscience, 33(5), 1940–1953.CrossRefPubMedGoogle Scholar
  13. Eckmann, J.P., Jacobi, S., Marom, S., Moses, E., & Zbinden, C. (2008). Leader neurons in population bursts of 2d living neural networks. New Journal of Physics, 10(1), 015,011.CrossRefGoogle Scholar
  14. Feinerman, O., Segal, M., & Moses, E. (2007). Identification and dynamics of spontaneous burst initiation zones in unidimensional neuronal cultures. Journal of Neurophysiology, 97(4), 2937–2948.CrossRefPubMedGoogle Scholar
  15. Gandolfo, M., Maccione, A., Tedesco, M., Martinoia, S., & Berdondini, L. (2010). Tracking burst patterns in hippocampal cultures with high-density CMOS-MEAs. Journal of Neural Engineering, 7(5), 056,001.CrossRefGoogle Scholar
  16. Gross, G.W., Williams, A.N., & Lucas, J.H. (1982). Recording of spontaneous activity with photoetched microelectrode surfaces from mouse spinal neurons in culture. Journal of Neuroscience Methods, 5(1), 13–22.CrossRefPubMedGoogle Scholar
  17. Harris, W.A. (1981). Neural activity and development. Annual Review of Physiology, 43(1), 689–710.CrossRefPubMedGoogle Scholar
  18. Holcman, D., & Tsodyks, M. (2006). The emergence of up and down states in cortical networks. PLOS Comput Biol, 2(3), e23.CrossRefPubMedPubMedCentralGoogle Scholar
  19. Hua, J.Y., & Smith, S.J. (2004). Neural activity and the dynamics of central nervous system development. Nature Neuroscience, 7(4), 327–332.CrossRefPubMedGoogle Scholar
  20. Jiruska, P., de Curtis, M., Jefferys, J.G.R., Schevon, C.A., Schiff, S.J., & Schindler, K. (2013). Synchronization and desynchronization in epilepsy: controversies and hypotheses. The Journal of Physiology, 591(4), 787–797.Google Scholar
  21. Johnson, H.A., & Buonomano, D.V. (2007). Development and plasticity of spontaneous activity and up states in cortical organotypic slices. The Journal of Neuroscience, 27(22), 5915–5925.CrossRefPubMedGoogle Scholar
  22. Katz, L.C., & Shatz, C.J. (1996). Synaptic activity and the construction of cortical circuits. Science, 274 (5290), 1133–1138.CrossRefPubMedGoogle Scholar
  23. Kerschensteiner, D. (2014). Spontaneous network activity and synaptic development. The Neuroscientist, 20 (3), 272–290.CrossRefPubMedGoogle Scholar
  24. Lau, P.M., & Bi, G.Q. (2005). Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proceedings of the National Academy of Sciences, 102(29), 10,333–10,338.CrossRefGoogle Scholar
  25. Lehnertz, K., Bialonski, S., Horstmann, M.T., Krug, D., Rothkegel, A., Staniek, M., & Wagner, T. (2009). Synchronization phenomena in human epileptic brain networks. Journal of Neuroscience Methods, 183(1), 42–48.CrossRefPubMedGoogle Scholar
  26. MacLean, J.N., Watson, B.O., Aaron, G.B., & Yuste, R. (2005). Internal dynamics determine the cortical response to thalamic stimulation. Neuron, 48(5), 811–823.CrossRefPubMedGoogle Scholar
  27. Maeda, E., Robinson, H.P.C., & Kawana, A. (1995). The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. Journal of Neuroscience, 15(10), 6834–6845.PubMedGoogle Scholar
  28. McCormick, D.A., & Contreras, D. (2001). On the cellular and network bases of epileptic seizures. Annual Review of Physiology, 63(1), 815–846.CrossRefPubMedGoogle Scholar
  29. Meister, M., Wong, R.O., Baylor, D.A., & Shatz, C.J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science, 252(5008), 939–943.CrossRefPubMedGoogle Scholar
  30. Mongillo, G., Barak, O., & Tsodyks, M. (2008). Synaptic theory of working memory. Science, 319(5869), 1543–1546.CrossRefPubMedGoogle Scholar
  31. Morris, C., & Lecar, H. (1981). Voltage oscillations in the barnacle giant muscle fiber. Biophysical Journal, 35(1), 193–213.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Orlandi, J.G., Soriano, J., Alvarez-Lacalle, E., Teller, S., & Casademunt, J. (2013). Noise focusing and the emergence of coherent activity in neuronal cultures. Nature Physics, 9(9), 582–590.CrossRefGoogle Scholar
  33. Penn, A.A., & Shatz, C.J. (1999). Brain waves and brain wiring: the role of endogenous and sensory-driven neural activity in development. Pediatric Research, 45(4, Part 1 of 2), 447–458.CrossRefPubMedGoogle Scholar
  34. Pine, J. (1980). Recording action potentials from cultured neurons with extracellular microcircuit electrodes. Journal of Neuroscience Methods, 2(1), 19–31.CrossRefPubMedGoogle Scholar
  35. Potter, S.M., & DeMarse, T.B. (2001). A new approach to neural cell culture for long-term studies. Journal of Neuroscience Methods, 110(1–2), 17–24.CrossRefPubMedGoogle Scholar
  36. Pu, J., Gong, H., Li, X., & Luo, Q. (2013). Developing neuronal networks: self-organized criticality predicts the future. Scientific Reports, 3.Google Scholar
  37. Raichman, N., & Ben-Jacob, E. (2008). Identifying repeating motifs in the activation of synchronized bursts in cultured neuronal networks. Journal of Neuroscience Methods, 170(1), 96– 110.CrossRefPubMedGoogle Scholar
  38. Schroeter, M.S., Charlesworth, P., Kitzbichler, M.G., Paulsen, O., & Bullmore, E.T. (2015). Emergence of rich-club topology and coordinated dynamics in development of hippocampal functional networks in vitro. The Journal of Neuroscience, 35(14), 5459–5470.Google Scholar
  39. Segev, R., Benveniste, M., Shapira, Y., & Ben-Jacob, E. (2003). Formation of electrically active clusterized neural networks. Physical Review Letters, 90(16), 168,101.CrossRefGoogle Scholar
  40. Thomas, C.A., Springer, P.A., Loeb, G.E., Berwald-Netter, Y., & Okun, L.M. (1972). A miniature microelectrode array to monitor the bioelectric activity of cultured cells. Experimental Cell Research, 74(1), 61–66.CrossRefPubMedGoogle Scholar
  41. Tsodyks, M.V., & Markram, H. (1997). The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proceedings of the National Academy of Sciences, 94(2), 719–723.CrossRefGoogle Scholar
  42. Turrigiano, G.G., & Nelson, S.B. (2004). Homeostatic plasticity in the developing nervous system. Nature Reviews Neuroscience, 5(2), 97–107.CrossRefPubMedGoogle Scholar
  43. Van Pelt, J., Corner, M.A., Wolters, P.S., Rutten, W.L.C., & Ramakers, G.J.A. (2004). Longterm stability and developmental changes in spontaneous network burst firing patterns in dissociated rat cerebral cortex cell cultures on multielectrode arrays. Neuroscience Letters, 361(1–3), 86–89.Google Scholar
  44. Volman, V., & Gerkin, R.C. (2011). Synaptic scaling stabilizes persistent activity driven by asynchronous neurotransmitter release. Neural Computation, 23(4), 927–957.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Volman, V., Gerkin, R.C., Lau, P.M., Ben-Jacob, E., & Bi, G.Q. (2007). Calcium and synaptic dynamics underlying reverberatory activity in neuronal networks. Physical Biology, 4(2), 91–103.CrossRefPubMedGoogle Scholar
  46. Wagenaar, D.A., Pine, J., & Potter, S.M. (2006). An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neuroscience, 7(1), 11.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Wang, X.J. (1999). Synaptic basis of cortical persistent activity: the importance of NMDA receptors to working memory. The Journal of Neuroscience, 19(21), 9587–9603.PubMedGoogle Scholar
  48. Wang, X.J. (2001). Synaptic reverberation underlying mnemonic persistent activity. Trends in Neurosciences, 24(8), 455–463.CrossRefPubMedGoogle Scholar
  49. Zhang, L.I., & Poo, MM (2001). Electrical activity and development of neural circuits. Nature Neuroscience, 4, 1207–1214.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Institute of PhysicsAcademia SinicaTaipeiRepublic of China
  2. 2.Department of Physics and Center for Complex SystemsNational Central UniversityChungliRepublic of China

Personalised recommendations