Combining microfluidics, optogenetics and calcium imaging to study neuronal communication in vitro

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Renault, Renaud ^a,b,c   Sukenik, Nirit ^c   Descroix, Stéphanie ^b   Malaquin, Laurent ^b   Viovy, Jean Louis ^b   Peyrin, Jean Michel ^d,e   Bottani, Samuel ^a   Monceau, Pascal ^a   Moses, Elisha ^c   Vignes, Maéva ^b,d,e,f  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b INSTITUT CURIE   (France)

^c WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^d Université Pierre et Marie Curie   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CHANNELRHODOPSIN 2; RHODOPSIN; UNCLASSIFIED DRUG; CALCIUM; CHANNELRHODOPSIN 2, RAT;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ARTICLE; CONNECTOME; EMBRYO; IN VITRO STUDY; MICROFLUIDICS; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NERVE FIBER GROWTH; NONHUMAN; OPTOGENETICS; PHOTOREACTIVITY; PROTEIN EXPRESSION; RAT; REFRACTORY PERIOD; SYNAPTIC TRANSMISSION; ANIMAL; AXON; CELL COMMUNICATION; CELL CULTURE; COMPUTER SIMULATION; CYTOLOGY; GENETICS; MAMMALIAN EMBRYO; METABOLISM; NERVE CELL; PHYSIOLOGY; PROCEDURES;

RODENTIA;

ANIMALS; AXONS; CALCIUM; CELL COMMUNICATION; CELLS, CULTURED; COMPUTER SIMULATION; EMBRYO, MAMMALIAN; IN VITRO TECHNIQUES; MICROFLUIDICS; NEURONS; OPTOGENETICS; RATS; RHODOPSIN;

EID: 84930627274     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120680     Document Type: Article

References (49)

1. Yang IH, Co CC, Ho CC (2011) Controlling neurite outgrowth with patterned substrates. Journal of Biomedical Materials Research Part A 97: 451-456. doi: 10.1002/jbm.a.33082 PMID: 21484989
2. Roth S, Bisbal M, Brocard J, Bugnicourt G, Saoudi Y, Andrieux A, et al. (2012) How morphological constraints affect axonal polarity in mouse neurons. PloS one 7: e33623. doi: 10.1371/journal.pone.0033623 PMID: 22457779
3. Chao ZC, Bakkum DJ, Potter SM (2007) Region-specific network plasticity in simulated and living cortical networks: comparison of the center of activity trajectory (CAT) with other statistics. Journal of Neural Engineering 4: 294-308. doi: 10.1088/1741-2560/4/3/015 PMID: 17873432
4. Dranias MR, Ju H, Rajaram E, VanDongen AMJ (2013) Short-term memory in networks of dissociated cortical neurons. The Journal of neuroscience: the official journal of the Society for Neuroscience 33: 1940-53. doi: 10.1523/JNEUROSCI.2718-12.2013
5. Feinerman O, Segal M, Moses E (2005) Signal propagation along unidimensional neuronal networks. Journal of neurophysiology 94: 3406-16. doi: 10.1152/jn.00264.2005 PMID: 16049148
6. Wagenaar DA, Pine J, Potter SM (2006) An extremely rich repertoire of bursting patterns during the development of cortical cultures. BMC Neuroscience 7: 11. doi: 10.1186/1471-2202-7-11 PMID: 16464257
7. 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 93: 41-53. doi: 10.1016/j.brainres.2006.03.049
8. Breskin I, Soriano J, Moses E, Tlusty T (2006) Percolation in Living Neural Networks. Physical Review Letters 97: 188102. doi: 10.1103/PhysRevLett.97.188102 PMID: 17155581
9. Hinard V, Mikhail C, Pradervand S, Curie T, Houtkooper RH, Auwerx J, et al. (2012) Key electrophysiological, molecular, and metabolic signatures of sleep and wakefulness revealed in primary cortical cultures. The Journal of neuroscience 32: 12506-17. doi: 10.1523/JNEUROSCI.2306-12.2012 PMID: 22956841
10. Marconi E, Nieus T, Maccione A, Valente P, Simi A, Messa M, et al. (2012) Emergent functional properties of neuronal networks with controlled topology. PloS one 7: e34648. doi: 10.1371/journal.pone.0034648 PMID: 22493706
11. Baruchi I, Ben-Jacob E (2007) Towards neuro-memory-chip: Imprinting multiple memories in cultured neural networks. Physical Review E 75: 1-4. doi: 10.1103/PhysRevE.75.050901
12. Bonifazi P, Ruaro ME, Torre V (2005) Statistical properties of information processing in neuronal networks. European Journal of Neuroscience 22: 2953-2964. doi: 10.1111/j.1460-9568.2005.04464.x PMID: 16324130
13. Feinerman O, Rotem A, Moses E (2008) Reliable neuronal logic devices from patterned hippocampal cultures. Nature Physics 4: 967-973. doi: 10.1038/nphys1099
14. Marx V (2014) Neurobiology: rethinking the electrode. Nature Methods 11: 1099-1103. doi: 10.1038/nmeth.3149
15. Morin F, Nishimura N, Griscom L, Lepioufle B, Fujita H, Takamura Y, et al. (2006) Constraining the connectivity of neuronal networks cultured on microelectrode arrays with microfluidic techniques: a step towards neuron-based functional chips. Biosensors & bioelectronics 21: 1093-100. doi: 10.1016/j.bios. 2005.04.020
16. Pan L, Alagapan S, Franca E, Brewer GJ, Wheeler BC (2011) Propagation of action potential activity in a predefined microtunnel neural network. Journal of neural engineering 8: 046031. doi: 10.1088/1741-2560/8/4/046031 PMID: 21750372
17. Kanagasabapathi TT, Ciliberti D, Martinoia S, Wadman WJ, Decr e MMJ (2011) Dual-compartment neurofluidic system for electrophysiological measurements in physically segregated and functionally connected neuronal cell culture. Frontiers in neuroengineering 4: 13. doi: 10.3389/fneng.2011.00013 PMID: 22025913
18. Brunello Ca, Jokinen V, Sakha P, Terazono H, Nomura F, Kaneko T, et al. (2013) Microtechnologies to fuel neurobiological research with nanometer precision. Journal of nanobiotechnology 11: 11. doi: 10.1186/1477-3155-11-11 PMID: 23575365
19. Zhang F, Wang LP, Brauner M, Liewald JF, Kay K, Watzke N, et al. (2007) Multimodal fast optical interrogation of neural circuitry. Nature 446: 633-639. doi: 10.1038/nature05744 PMID: 17410168
20. Yizhar O, Fenno LE, Davidson TJ, Mogri M, Deisseroth K (2011) Optogenetics in neural systems. Neuron 71: 9-34. doi: 10.1016/j.neuron.2011.06.004 PMID: 21745635
21. Bernstein J, Boyden E (2011) Optogenetic tools for analyzing the neural circuits of behavior. Trends in cognitive sciences 15: 592-600. doi: 10.1016/j.tics.2011.10.003 PMID: 22055387
22. Madisen L, Mao T, Koch H, Zhuo Jm (2012) A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nature Neuroscience. doi: 10.1038/nn.3078 PMID: 22446880
23. Papagiakoumou E, Anselmi F, B egue A, de Sars V, Gluckstad J, Isacoff E, et al. (2010) Scanless twophoton excitation of channelrhodopsin-2.Nature Methods 7: 848-854. doi: 10.1038/nmeth.1505 PMID: 20852649
24. Anselmi F, Ventalon C, B egue A, Ogden D, Emiliani V (2011)Three-dimensional imaging and photostimulation by remote-focusing and holographic light patterning. Proceedings of the National Academy of Sciences of the United States of America 108: 19504-9. doi: 10.1073/pnas.1109111108 PMID: 22074779
25. Valley M, Wagner S, Gallarda BW, Lledo PM (2011) Using affordable LED arrays for photo-stimulation of neurons. Journal of visualized experiments JoVE: 2-5.
26. Smetters D, Majewska A, Yuste R (1999) Detecting action potentials in neuronal populations with calcium imaging. Methods 18: 215-21. doi: 10.1006/meth.1999.0774 PMID: 10356353
27. Miyawaki A, Griesbeck O, Heim R, Tsien RY (1999) Dynamic and quantitative Ca2 measurements using improved cameleons. Proceedings of the National Academy of Sciences 96: 2135. doi: 10.1073/pnas.96.5.2135
28. Göbel W, Helmchen F (2007) In vivo calcium imaging of neural network function. Physiology 22: 358-65. doi: 10.1152/physiol.00032.2007 PMID: 18073408
29. Mohanty SK, Reinscheid RK, Liu X, Okamura N, Krasieva TB, Berns M. (2008) In-Depth Activation of Channelrhodopsin 2-Sensitized Excitable Cells with High Spatial Resolution Using Two-Photon Excitation with a Near-Infrared Laser Microbeam Cell culture. Biophysical journal 95: 3916-3926. doi: 10. 1529/biophysj.108.130187 PMID: 18621808
30. Bernardinelli Y, Salmon C, Jones EV, Farmer WT, Stellwagen D, Murai KK. (2011) Astrocytes Display Complex and Localized Calcium Responses to Single-Neuron Stimulation in the Hippocampus. The Journal of neuroscience 31: 8905-8919. doi: 10.1523/JNEUROSCI.6341-10.2011 PMID: 21677174
31. Lin JY, Lin MZ, Steinbach P, Tsien RY (2009) Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophysical journal 96: 1803-1814. doi: 10.1016/j.bpj.2008.11.034 PMID: 19254539
32. Yuste R, MacLean J, Vogelstein J, Paninski L (2011) Imaging action potentials with calcium indicators. Cold Spring Harbor protocols 2009: pdb.prot5316.
33. Gradinaru V, Thompson KR, Zhang F, Mogri M, Kay K, Schneider MB, et al. (2007) Targeting and readout strategies for fast optical neural control in vitro and in vivo. The Journal of neuroscience: the official journal of the Society for Neuroscience 27: 14231-8. doi: 10.1523/JNEUROSCI.3578-07.2007
34. Stenger Da, Hickman JJ, Bateman KE, Ravenscroft MS, Ma W, Pancrazio J, et al. (1998) Microlithographic determination of axonal/dendritic polarity in cultured hippocampal neurons. Journal of Neuroscience Methods 82: 167-173. doi: 10.1016/S0165-0270(98)00047-8 PMID: 9700689
35. Vogt AK, Stefani FD, Best A, Nelles G, Yasuda A, Knoll W, et al. (2004) Impact of micropatterned surfaces on neuronal polarity. Journal of neuroscience methods 134: 191-8. doi: 10.1016/j.jneumeth. 2003.11.004 PMID: 15003385
36. Taylor AM, Blurton-jones M, Rhee SW, Cribbs DH, Cotman CW (2005) A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nature Methods 2: 599-605. doi: 10.1038/nmeth777 PMID: 16094385
37. Park JW, Kim HJ, Kang MW, Jeon NL (2013) Advances in microfluidics-based experimental methods for neuroscience research. Lab on a chip 13: 509-21. doi: 10.1039/c2lc41081h PMID: 23306275
38. Pautot S, Wyart C, Isacoff EY (2008) Colloid-guided assembly of oriented 3D neuronal networks. Nature Methods 5: 735-740. doi: 10.1038/NMETH.1236 PMID: 18641658
39. Hallstrom W, Prinz CN, Suyatin D, Samuelson L, Montelius L, Kanje M. (2009) Rectifying and Sorting of Regenerating Axons by Free-Standing Nanowire Patterns: A Highway for Nerve Fibers. Langmuir 25: 4343-4346. doi: 10.1021/la900436e PMID: 19296620
40. Hattori S, Suzurikawa J, Kanzaki R, Jimbo Y, Hamaguchi T, Takahashi H, et al. (2010) Direction control of information transfer between neuronal populations with asymmetric three-dimensional microstructure. Electronics and Communications in Japan 93: 17-25. doi: 10.1002/ecj.10240
41. Taylor AM, Dieterich DC, Ito HT, Kim Sa, Schuman EM (2010) Microfluidic local perfusion chambers for the visualization and manipulation of synapses. Neuron 66: 57-68. doi: 10.1016/j.neuron.2010.03.022 PMID: 20399729
42. Peyrin JM, Deleglise B, Saias L, Vignes M, Gougis P, Magnifico S, et al. (2011) Axon diodes for the reconstruction of oriented neuronal networks in microfluidic chambers. Lab on a Chip 11: 3663-3673. doi: 10.1039/c1lc20014c PMID: 21922081
43. Roth S, Bugnicourt G, Bisbal M, Gory-Faur e S, Brocard J, Villard C. (2012) Neuronal architectures with axo-dendritic polarity above silicon nanowires. Small 8: 671-5. doi: 10.1002/smll.201102325 PMID: 22228548
44. Odawara A, Gotoh M, Suzuki I (2013) Control of neural network patterning using collagen gel photothermal etching. Lab on a chip 13: 2040-6. doi: 10.1039/c3lc00036b PMID: 23615759
45. Orlandi JG, Soriano J, Alvarez-Lacalle E, Teller S, Casademunt J (2013) Noise focusing and the emergence of coherent activity in neuronal cultures. Nature Physics 9: 582-590. doi: 10.1038/nphys2686
46. Teller S, Granell C, De Domenico M, Soriano J, G omez S, Arenas A. (2014) Emergence of assortative mixing between clusters of cultured neurons. PLoS computational biology 10: e1003796. doi: 10.1371/journal.pcbi.1003796 PMID: 25188377
47. Goldin M, Segal M, Avignone E (2001) Functional plasticity triggers formation and pruning of dendritic spines in cultured hippocampal networks. The Journal of Neuroscience 21: 186-193. PMID: 11150335
48. Nathanson J, Yanagawa Y, Obata K, Callaway E (2009) Preferential labeling of inhibitory and excitatory cortical neurons by endogenous tropism of AAV and lentiviral vectors. Neuroscience 161: 441-450. doi: 10.1016/j.neuroscience.2009.03.032 PMID: 19318117
49. Cohen O, Keselman A, Moses E, Rodr guez-Mart nez M, Soriano J, Tlusty T. (2010) Quorum percolation in living neural networks. Europhysics Letters 89: 18008. doi: 10.1209/0295-5075/89/18008