Brief wide-field photostimuli evoke and modulate oscillatory reverberating activity in cortical networks

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Pulizzi, Rocco ^a   Musumeci, Gabriele ^a   Van Den Haute, Chris ^b,c   Van De Vijver, Sebastiaan ^a   Baekelandt, Veerle ^b   Giugliano, Michele ^a,d,e  

^a UNIVERSITY OF ANTWERP   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c KU LEUVEN   (Belgium)

^d UNIVERSITY OF SHEFFIELD   (United Kingdom)

^e EPFL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; OPSIN;

ANIMAL; BIOLOGICAL MODEL; BRAIN CORTEX; CELL CULTURE; EVOKED RESPONSE; GAMMA RHYTHM; GENE EXPRESSION; GENETICS; IN VITRO STUDY; LIGHT; METABOLISM; NERVE CELL; NERVE TRACT; PHOTOSTIMULATION; PHYSIOLOGY; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; EVOKED POTENTIALS; GAMMA RHYTHM; GENE EXPRESSION; IN VITRO TECHNIQUES; LIGHT; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; OPSINS; PHOTIC STIMULATION; RATS; RECEPTORS, GABA-A; SYNAPTIC TRANSMISSION;

EID: 84964666302     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep24701     Document Type: Article

References (93)

1. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature neuroscience 8, 1263-1268, doi: 10. 1038/nn1525 (2005).
2. Deisseroth, K. et al. Next-generation optical technologies for illuminating genetically targeted brain circuits. The Journal of neuroscience: the official journal of the Society for Neuroscience 26, 10380-10386, doi: 10. 1523/JNEUROSCI. 3863-06. 2006 (2006).
3. Williams, S. C. & Deisseroth, K. Optogenetics. Proceedings of the National Academy of Sciences of the United States of America 110, 16287, doi: 10. 1073/pnas. 1317033110 (2013).
4. Fenno, L., Yizhar, O. & Deisseroth, K. The development and application of optogenetics. Annual review of neuroscience 34, 389-412, doi: 10. 1146/annurev-neuro-061010-113817 (2011).
5. Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M. & Deisseroth, K. Optogenetics in neural systems. Neuron 71, 9-34, doi: 10. 1016/j. neuron. 2011. 06. 004 (2011).
6. Boyden, E. S. A history of optogenetics: the development of tools for controlling brain circuits with light. F1000 Biol Rep 3, 11, doi: 10. 3410/B3-11 (2011).
7. Boyden, E. S. Optogenetics: using light to control the brain. Cerebrum 2011, 16 (2011).
8. Hausser, M. Optogenetics: the age of light. Nat Methods 11, 1012-1014, doi: 10. 1038/nmeth. 3111 (2014).
9. Liu, X. et al. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484, 381-385, doi: 10. 1038/nature11028 (2012).
10. Bernstein, J. G. & Boyden, E. S. Optogenetic tools for analyzing the neural circuits of behavior. Trends in cognitive sciences 15, 592-600, doi: 10. 1016/j. tics. 2011. 10. 003 (2011).
11. Dranias, M. R., Ju, H., Rajaram, E. & VanDongen, A. M. Short-term memory in networks of dissociated cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 33, 1940-1953, doi: 10. 1523/JNEUROSCI. 2718-12. 2013 (2013).
12. El Hady, A. et al. Optogenetic stimulation effectively enhances intrinsically generated network synchrony. Frontiers in neural circuits 7, 167, doi: 10. 3389/fncir. 2013. 00167 (2013).
13. Inagaki, H. K. et al. Optogenetic control of Drosophila using a red-shifted channelrhodopsin reveals experience-dependent influences on courtship. Nat Methods 11, 325-332, doi: 10. 1038/nmeth. 2765 (2014).
14. Roux, L., Stark, E., Sjulson, L. & Buzsaki, G. In Vivo optogenetic identification and manipulation of GABAergic interneuron subtypes. Current opinion in neurobiology 26, 88-95, doi: 10. 1016/j. conb. 2013. 12. 013 (2014).
15. Tchumatchenko, T., Newman, J. P., Fong, M. F. & Potter, S. M. Delivery of continuously-varying stimuli using channelrhodopsin-2. Frontiers in neural circuits 7, 184, doi: 10. 3389/fncir. 2013. 00184 (2013).
16. Malyshev, A., Goz, R., LoTurco, J. J. & Volgushev, M. Advantages and limitations of the use of optogenetic approach in studying fastscale spike encoding. PloS one 10, e0122286, doi: 10. 1371/journal. pone. 0122286 (2015).
17. Vaziri, A. & Emiliani, V. Reshaping the optical dimension in optogenetics. Current opinion in neurobiology 22, 128-137, doi: 10. 1016/j. conb. 2011. 11. 011 (2012).
18. Schoenenberger, P., Grunditz, A., Rose, T. & Oertner, T. G. Optimizing the spatial resolution of Channelrhodopsin-2 activation. Brain Cell Biol 36, 119-127, doi: 10. 1007/s11068-008-9025-8 (2008).
19. Petreanu, L., Huber, D., Sobczyk, A. & Svoboda, K. Channelrhodopsin-2-assisted circuit mapping of long-range callosal projections. Nature neuroscience 10, 663-668, doi: 10. 1038/nn1891 (2007).
20. Gradinaru, V., Mogri, M., Thompson, K. R., Henderson, J. M. & Deisseroth, K. Optical deconstruction of parkinsonian neural circuitry. Science 324, 354-359, doi: 10. 1126/science. 1167093 (2009).
21. Lau, P. M. & Bi, G. Q. Synaptic mechanisms of persistent reverberatory activity in neuronal networks. Proceedings of the National Academy of Sciences of the United States of America 102, 10333-10338, doi: 10. 1073/pnas. 0500717102 (2005).
22. Eytan, D. & Marom, S. Dynamics and effective topology underlying synchronization in networks of cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 26, 8465-8476, doi: 10. 1523/JNEUROSCI. 1627-06. 2006 (2006).
23. Tateno, T., Jimbo, Y. & Robinson, H. P. Spatio-temporal cholinergic modulation in cultured networks of rat cortical neurons: spontaneous activity. Neuroscience 134, 425-437, doi: 10. 1016/j. neuroscience. 2005. 04. 049 (2005).
24. Rieubland, S., Roth, A. & Hausser, M. Structured connectivity in cerebellar inhibitory networks. Neuron 81, 913-929, doi: 10. 1016/j. neuron. 2013. 12. 029 (2014).
25. Barak, O., Tsodyks, M. & Romo, R. Neuronal population coding of parametric working memory. The Journal of neuroscience: the official journal of the Society for Neuroscience 30, 9424-9430, doi: 10. 1523/JNEUROSCI. 1875-10. 2010 (2010).
26. Grossman, N. et al. The spatial pattern of light determines the kinetics and modulates backpropagation of optogenetic action potentials. Journal of computational neuroscience 34, 477-488, doi: 10. 1007/s10827-012-0431-7 (2012).
27. Witt, A. et al. Controlling the oscillation phase through precisely timed closed-loop optogenetic stimulation: a computational study. Frontiers in neural circuits 7, doi: 10. 3389/fncir. 2013. 00049 (2013).
28. Williams, J. C. et al. Computational optogenetics: empirically-derived voltage-and light-sensitive channelrhodopsin-2 model. PLoS computational biology 9, e1003220, doi: 10. 1371/journal. pcbi. 1003220 (2013).
29. Gal, A. et al. Dynamics of Excitability over Extended Timescales in Cultured Cortical Neurons. Journal of Neuroscience 30, 16332-16342, doi: 10. 1523/jneurosci. 4859-10. 2010 (2010).
30. Reinartz, S., Biro, I., Gal, A., Giugliano, M. & Marom, S. Synaptic dynamics contribute to long-term single neuron response fluctuations. Frontiers in neural circuits 8, doi: 10. 3389/fncir. 2014. 00071 (2014).
31. Marom, S. & Eytan, D. Learning in ex-vivo developing networks of cortical neurons. Progress in brain research 147, 189-199, doi: 10. 1016/S0079-6123(04)47014-9 (2005).
32. Corner, M. A., van Pelt, J., Wolters, P. S., Baker, R. E. & Nuytinck, R. H. Physiological effects of sustained blockade of excitatory synaptic transmission on spontaneously active developing neuronal networks-an inquiry into the reciprocal linkage between intrinsic biorhythms and neuroplasticity in early ontogeny. Neurosci Biobehav Rev 26, 127-185 (2002).
33. Potter, S. M. & DeMarse, T. B. A new approach to neural cell culture for long-term studies. Journal of neuroscience methods 110, 17-24 (2001).
34. Marom, S. & Shahaf, G. Development, learning and memory in large random networks of cortical neurons: lessons beyond anatomy. Quarterly reviews of biophysics 35, 63-87 (2002).
35. Pine, J. Recording action potentials from cultured neurons with extracellular microcircuit electrodes. Journal of neuroscience methods 2, 19-31 (1980).
36. Gross, G. W., Williams, A. N. & Lucas, J. H. Recording of spontaneous activity with photoetched microelectrode surfaces from mouse spinal neurons in culture. Journal of neuroscience methods 5, 13-22 (1982).
37. Wagenaar, D. A., Pine, J. & Potter, S. M. Effective parameters for stimulation of dissociated cultures using multi-electrode arrays. Journal of neuroscience methods 138, 27-37, doi: 10. 1016/j. jneumeth. 2004. 03. 005 (2004).
38. Jimbo, Y., Kawana, A., Parodi, P. & Torre, V. The dynamics of a neuronal culture of dissociated cortical neurons of neonatal rats. Biological cybernetics 83, 1-20 (2000).
39. Buzsaki, G. & Wang, X. J. Mechanisms of gamma oscillations. Annual review of neuroscience 35, 203-225, doi: 10. 1146/annurevneuro-062111-150444 (2012).
40. Liu, X. B. & Murray, K. D. Neuronal excitability and calcium/calmodulin-dependent protein kinase type II: location, location, location. Epilepsia 53 Suppl 1, 45-52, doi: 10. 1111/j. 1528-1167. 2012. 03474. x (2012).
41. Prigge, M. et al. Color-tuned channelrhodopsins for multiwavelength optogenetics. The Journal of biological chemistry 287, 31804-31812, doi: 10. 1074/jbc. M112. 391185 (2012).
42. van Pelt, J., Wolters, P. S., Corner, M. A., Rutten, W. L. & Ramakers, G. J. Long-term characterization of firing dynamics of spontaneous bursts in cultured neural networks. IEEE transactions on bio-medical engineering 51, 2051-2062, doi: 10. 1109/TBME. 2004. 827936 (2004).
43. Chiappalone, M., Massobrio, P. & Martinoia, S. Network plasticity in cortical assemblies. The European journal of neuroscience 28, 221-237, doi: 10. 1111/j. 1460-9568. 2008. 06259. x (2008).
44. Koch, C. & Segev, I. Methods in Neuronal Modeling: From Ions to Networks. (MIT Press, 1998).
45. Shein Idelson, M., Ben-Jacob, E. & Hanein, Y. Innate synchronous oscillations in freely-organized small neuronal circuits. PloS one 5, e14443, doi: 10. 1371/journal. pone. 0014443 (2010).
46. Giugliano, M., Darbon, P., Arsiero, M., Luscher, H. R. & Streit, J. Single-neuron discharge properties and network activity in dissociated cultures of neocortex. Journal of neurophysiology 92, 977-996, doi: 10. 1152/jn. 00067. 2004 (2004).
47. Gullo, F. et al. Orchestration of "presto" and "largo" synchrony in up-down activity of cortical networks. Frontiers in neural circuits 4, 11, doi: 10. 3389/fncir. 2010. 00011 (2010).
48. Wilson, H. R. & Cowan, J. D. Excitatory and inhibitory interactions in localized populations of model neurons. Biophysical journal 12, 1-24, doi: 10. 1016/S0006-3495(72)86068-5 (1972).
49. Oppenheim, A. V., Schafer, R. W. & Buck, J. R. Discrete-time signal processing (2nd ed. ). (Prentice-Hall, Inc., 1999).
50. Markram, H., Lubke, J., Frotscher, M. & Sakmann, B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275, 213-215 (1997).
51. Zucker, R. S. & Regehr, W. G. Short-term synaptic plasticity. Annual review of physiology 64, 355-405, doi: 10. 1146/annurev. physiol. 64. 092501. 114547 (2002).
52. Turrigiano, G. G., Leslie, K. R., Desai, N. S., Rutherford, L. C. & Nelson, S. B. Activity-dependent scaling of quantal amplitude in neocortical neurons. Nature 391, 892-896, doi: 10. 1038/36103 (1998).
53. Prange, O. & Murphy, T. H. Correlation of miniature synaptic activity and evoked release probability in cultures of cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 19, 6427-6438 (1999).
54. Lou, X., Scheuss, V. & Schneggenburger, R. Allosteric modulation of the presynaptic Ca2+ sensor for vesicle fusion. Nature 435, 497-501, doi: 10. 1038/nature03568 (2005).
55. Kochubey, O., Lou, X. & Schneggenburger, R. Regulation of transmitter release by Ca(2+ ) and synaptotagmin: insights from a large CNS synapse. Trends in neurosciences 34, 237-246, doi: 10. 1016/j. tins. 2011. 02. 006 (2011).
56. Plenz, D. & Kitai, S. T. Generation of high-frequency oscillations in local circuits of rat somatosensory cortex cultures. Journal of neurophysiology 76, 4180-4184 (1996).
57. Cunningham, M. O. et al. A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. Proceedings of the National Academy of Sciences of the United States of America 101, 7152-7157, doi: 10. 1073/pnas. 0402060101 (2004).
58. Gireesh, E. D. & Plenz, D. Neuronal avalanches organize as nested theta-and beta/gamma-oscillations during development of cortical layer 2/3. Proceedings of the National Academy of Sciences of the United States of America 105, 7576-7581, doi: 10. 1073/pnas. 0800537105 (2008).
59. Thut, G., Miniussi, C. & Gross, J. The functional importance of rhythmic activity in the brain. Current biology: CB 22, R658-663, doi: 10. 1016/j. cub. 2012. 06. 061 (2012).
60. Basar, E. & Guntekin, B. A review of brain oscillations in cognitive disorders and the role of neurotransmitters. Brain research 1235, 172-193, doi: 10. 1016/j. brainres. 2008. 06. 103 (2008).
61. Mattia, M. & Del Giudice, P. Population dynamics of interacting spiking neurons. Physical review. E, Statistical, nonlinear, and soft matter physics 66, 051917 (2002).
62. Knight, B. W., Omurtag, A. & Sirovich, L. The approach of a neuron population firing rate to a new equilibrium: an exact theoretical result. Neural computation 12, 1045-1055 (2000).
63. Mainen, Z. F. & Sejnowski, T. J. Reliability of spike timing in neocortical neurons. Science 268, 1503-1506 (1995).
64. Brunel, N. & Wang, X. J. What Determines the Frequency of Fast Network Oscillations With Irregular Neural Discharges? I. Synaptic Dynamics and Excitation-Inhibition Balance. Journal of neurophysiology, 415-430, doi: 10. 1152/jn. 01095. 2002 (2003).
65. Wang, X. J. Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90, 1195-1268, doi: 10. 1152/physrev. 00035. 2008 (2010).
66. Van der Perren, A. et al. Efficient and stable transduction of dopaminergic neurons in rat substantia nigra by rAAV 2/1, 2/2, 2/5, 2/6. 2, 2/7, 2/8 and 2/9. Gene therapy 18, 517-527, doi: 10. 1038/gt. 2010. 179 (2011).
67. Linaro, D., Couto, J. & Giugliano, M. Command-line cellular electrophysiology for conventional and real-time closed-loop experiments. Journal of neuroscience methods 230, 5-19, doi: 10. 1016/j. jneumeth. 2014. 04. 003 (2014).
68. Zhang, Y. P. & Oertner, T. G. Optical induction of synaptic plasticity using a light-sensitive channel. Nat Methods 4, 139-141, doi: 10. 1038/nmeth988 (2007).
69. Mahmud, M., Pulizzi, R., Vasilaki, E. & Giugliano, M. QSpike tools: a generic framework for parallel batch preprocessing of extracellular neuronal signals recorded by substrate microelectrode arrays. Frontiers in neuroinformatics 8, 26, doi: 10. 3389/fninf. 2014. 00026 (2014).
70. Chance, F. S., Abbott, L. F. & Reyes, A. D. Gain modulation from background synaptic input. Neuron 35, 773-782 (2002).
71. Klapoetke, N. C. et al. Independent optical excitation of distinct neural populations. Nat Methods 11, 338-346, doi: 10. 1038/nmeth. 2836 (2014).
72. Haroush, N. & Marom, S. Slow dynamics in features of synchronized neural network responses. Frontiers in computational neuroscience 9, 40, doi: 10. 3389/fncom. 2015. 00040 (2015).
73. Hegemann, P. & Nagel, G. From channelrhodopsins to optogenetics. EMBO Mol Med 5, 173-176, doi: 10. 1002/emmm. 201202387 (2013).
74. Grubb, M. S. & Burrone, J. Channelrhodopsin-2 localised to the axon initial segment. PloS one 5, e13761, doi: 10. 1371/journal. pone. 0013761 (2010).
75. Droge, M. H., Gross, G. W., Hightower, M. H. & Czisny, L. E. Multielectrode analysis of coordinated, multisite, rhythmic bursting in cultured cns monolayer networks. The Journal of neuroscience: the official journal of the Society for Neuroscience 6, 1583-1592 (1986).
76. Jimbo, Y., Robinson, H. P. & Kawana, A. Simultaneous measurement of intracellular calcium and electrical activity from patterned neural networks in culture. IEEE Transactions in Biomedical Engineering 40, 804-810. doi: 10. 1109/10. 238465 (1993).
77. Maeda, E., Robinson, H. P. & Kawana, A. The mechanisms of generation and propagation of synchronized bursting in developing networks of cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 15, 6834-6845 (1995).
78. Shahaf, G. & Marom, S. Learning in networks of cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 21, 8782-8788 (2001).
79. Wagenaar, D. A., Pine, J. & Potter, S. M. An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neuroscience 7, 11, doi: 10. 1186/1471-2202-7-11 (2006).
80. Ham, M. I., Bettencourt, L. M., McDaniel, F. D. & Gross, G. W. Spontaneous coordinated activity in cultured networks: analysis of multiple ignition sites, primary circuits, and burst phase delay distributions. Journal of Computational Neuroscience 24, 346-357, doi: 10. 1007/s10827-007-0059-1 (2008).
81. Stegenga, J., le Feber, J. & Rutten, W. L. C. Changes within bursts during learning in dissociated neural networks. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2008, 4968-4971, doi: 10. 1109/IEMBS. 2008. 4650329 (2008).
82. Einevoll, G. T., Kayser, C., Logothetis, N. K. & Panzeri, S. Modelling and analysis of local field potentials for studying the function of cortical circuits. Nature Reviews Neuroscience 14, 770-785, doi: 10. 1038/nrn3599 (2013).
83. Waldert, S., Lemon, R. N. & Kraskov, A. Influence of spiking activity on cortical local field potentials. Journal of Physiology 591. 21, 5291-5303 (2013).
84. Wagenaar, D. A., Madhavan, R., Pine, J. & Potter, S. M. Controlling bursting in cortical cultures with closed-loop multi-electrode stimulation. The Journal of neuroscience: the official journal of the Society for Neuroscience 25, 680-688, doi: 10. 1523/JNEUROSCI. 4209-04. 2005 (2005).
85. Press, W. H., Teukolsky, S. A., Vetterling, W. T. & Flannery, B. P. Numerical Recipes 3rd Edition: The Art of Scientific Computing. (Cambridge University Press, 2007).
86. Newman, J. P. et al. Optogenetic feedback control of neural activity. Elife 4, doi: 10. 7554/eLife. 07192 (2015).
87. Brette, R. et al. High-resolution intracellular recordings using a real-time computational model of the electrode. Neuron 59, 379-391, doi: 10. 1016/j. neuron. 2008. 06. 021 (2008).
88. Quiroga, R. What is the real shape of extracellular spikes? Journal of neuroscience methods 177, 194-198, doi: 10. 1016/j. jneumeth. 2008. 09. 033 (2009).
89. Quiroga, R. Q. Spike sorting. Current biology: CB 22, R45-46, doi: 10. 1016/j. cub. 2011. 11. 005 (2012).
90. Quiroga, R. Q., Nadasdy, Z. & Ben-Shaul, Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural computation 16, 1661-1687, doi: 10. 1162/089976604774201631 (2004).
91. Mattia, M., Ferraina, S. & Del Giudice, P. In NeuroImage Vol. 52, 812-823 (2010).
92. Dayan, P. & Abbott, L. F. Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems. (The MIT Press, 2005).
93. Brogan, W. L. Modern control theory (3rd ed. ). (Prentice-Hall, Inc., 1991).