{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,14]],"date-time":"2026-04-14T02:13:39Z","timestamp":1776132819537,"version":"3.50.1"},"reference-count":60,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2017,10,27]],"date-time":"2017-10-27T00:00:00Z","timestamp":1509062400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2017,10,27]],"date-time":"2017-10-27T00:00:00Z","timestamp":1509062400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Ultra-sensitive electrodes for extracellular recordings were fabricated and electrically characterized. A signal detection limit defined by a noise level of 0.3\u20130.4 \u03bcV for a bandwidth of 12.5\u2009Hz was achieved. To obtain this high sensitivity, large area (4 mm<jats:sup>2<\/jats:sup>) electrodes were used. The electrode surface is also micro-structured with an array of gold mushroom-like shapes to further enhance the active area. In comparison with a flat gold surface, the micro-structured surface increases the capacitance of the electrode\/electrolyte interface by 54%. The electrode low impedance and low noise enable the detection of weak and low frequency quasi-periodic signals produced by astrocytes populations that thus far had remained inaccessible using conventional extracellular electrodes. Signals with 5 \u03bcV in amplitude and lasting for 5\u201310\u2009s were measured, with a peak-to-peak signal-to-noise ratio of 16. The electrodes and the methodology developed here can be used as an ultrasensitive electrophysiological tool to reveal the synchronization dynamics of ultra-slow ionic signalling between non-electrogenic cells.<\/jats:p>","DOI":"10.1038\/s41598-017-14697-y","type":"journal-article","created":{"date-parts":[[2017,10,23]],"date-time":"2017-10-23T20:17:15Z","timestamp":1508789835000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Ultrasensitive gold micro-structured electrodes enabling the detection of extra-cellular long-lasting potentials in astrocytes populations"],"prefix":"10.1038","volume":"7","author":[{"given":"Ana L. G.","family":"Mestre","sequence":"first","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4278-5710","authenticated-orcid":false,"given":"M\u00f3nica","family":"Cerquido","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1986-7918","authenticated-orcid":false,"given":"Pedro M. C.","family":"In\u00e1cio","sequence":"additional","affiliation":[]},{"given":"Sanaz","family":"Asgarifar","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2882-6026","authenticated-orcid":false,"given":"Ana S.","family":"Louren\u00e7o","sequence":"additional","affiliation":[]},{"given":"Maria L. S.","family":"Cristiano","sequence":"additional","affiliation":[]},{"given":"Paulo","family":"Aguiar","sequence":"additional","affiliation":[]},{"given":"Maria C. R.","family":"Medeiros","sequence":"additional","affiliation":[]},{"given":"In\u00eas M.","family":"Ara\u00fajo","sequence":"additional","affiliation":[]},{"given":"Jo\u00e3o","family":"Ventura","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3664-4740","authenticated-orcid":false,"given":"Henrique L.","family":"Gomes","sequence":"additional","affiliation":[]}],"member":"297","published-online":{"date-parts":[[2017,10,27]]},"reference":[{"key":"14697_CR1","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1038\/nnano.2012.265","volume":"8","author":"ME Spira","year":"2013","unstructured":"Spira, M. E. & Hai, A. Multi-electrode array technologies for neuroscience and cardiology. Nat. Nanotechnol. \n                           8, 83\u201394 (2013).","journal-title":"Nat. Nanotechnol."},{"key":"14697_CR2","doi-asserted-by":"publisher","first-page":"423","DOI":"10.3389\/fnins.2014.00423","volume":"8","author":"MEJ Obien","year":"2015","unstructured":"Obien, M. E. J., Deligkaris, K., Bullmann, T., Bakkum, D. J. & Frey, U. Revealing neuronal function through microelectrode array recordings. Front. Neurosci. \n                           8, 423 (2015).","journal-title":"Front. Neurosci."},{"key":"14697_CR3","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1109\/JPROC.2010.2066532","volume":"99","author":"A Hierlemann","year":"2011","unstructured":"Hierlemann, A., Frey, U., Hafizovic, S. & Heer, F. Growing Cells Atop Microelectronic Chips: Interfacing Electrogenic Cells In Vitro With CMOS-Based Microelectrode Arrays. Proc. IEEE \n                           99, 252\u2013284 (2011).","journal-title":"Proc. IEEE"},{"key":"14697_CR4","doi-asserted-by":"publisher","first-page":"38","DOI":"10.3389\/fncir.2013.00038","volume":"7","author":"JT Robinson","year":"2013","unstructured":"Robinson, J. T., Jorgolli, M. & Park, H. Nanowire electrodes for high-density stimulation and measurement of neural circuits. Front. Neural Circuits \n                           7, 38 (2013).","journal-title":"Front. Neural Circuits"},{"key":"14697_CR5","doi-asserted-by":"publisher","first-page":"914","DOI":"10.1021\/nl900096z","volume":"9","author":"BP Timko","year":"2009","unstructured":"Timko, B. P. et al. Electrical recording from hearts with flexible nanowire device arrays. Nano Lett. \n                           9, 914\u2013918 (2009).","journal-title":"Nano Lett."},{"key":"14697_CR6","doi-asserted-by":"publisher","first-page":"434","DOI":"10.1038\/nnano.2008.174","volume":"3","author":"EW Keefer","year":"2008","unstructured":"Keefer, E. W., Botterman, B. R., Romero, M. I., Rossi, A. F. & Gross, G. W. Carbon nanotube coating improves neuronal recordings. Nat. Nanotechnol. \n                           3, 434\u2013439 (2008).","journal-title":"Nat. Nanotechnol."},{"key":"14697_CR7","doi-asserted-by":"publisher","first-page":"6931","DOI":"10.1523\/JNEUROSCI.1051-07.2007","volume":"27","author":"A Mazzatenta","year":"2007","unstructured":"Mazzatenta, A. et al. Interfacing neurons with carbon nanotubes: electrical signal transfer and synaptic stimulation in cultured brain circuits. J. Neurosci. \n                           27, 6931\u20136 (2007).","journal-title":"J. Neurosci."},{"key":"14697_CR8","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1007\/s10544-008-9255-7","volume":"11","author":"M Shein","year":"2009","unstructured":"Shein, M. et al. Engineered neuronal circuits shaped and interfaced with carbon nanotube microelectrode arrays. Biomed. Microdevices \n                           11, 495\u2013501 (2009).","journal-title":"Biomed. Microdevices"},{"key":"14697_CR9","doi-asserted-by":"publisher","first-page":"2135","DOI":"10.1002\/adma.201204322","volume":"25","author":"M Sessolo","year":"2013","unstructured":"Sessolo, M. et al. Easy-to-Fabricate Conducting Polymer Microelectrode Arrays. Adv. Mater. \n                           25, 2135\u20132139 (2013).","journal-title":"Adv. Mater."},{"key":"14697_CR10","doi-asserted-by":"publisher","first-page":"L6","DOI":"10.1088\/1741-2560\/4\/2\/L02","volume":"4","author":"SM Richardson-Burns","year":"2007","unstructured":"Richardson-Burns, S. M., Hendricks, J. L. & Martin, D. C. Electrochemical polymerization of conducting polymers in living neural tissue. J. Neural Eng. \n                           4, L6\u2013L13 (2007).","journal-title":"J. Neural Eng."},{"key":"14697_CR11","doi-asserted-by":"publisher","first-page":"16","DOI":"10.1016\/j.jneumeth.2006.08.008","volume":"160","author":"T Nyberg","year":"2007","unstructured":"Nyberg, T., Shimada, A. & Torimitsu, K. Ion conducting polymer microelectrodes for interfacing with neural networks. J. Neurosci. Methods \n                           160, 16\u201325 (2007).","journal-title":"J. Neurosci. Methods"},{"key":"14697_CR12","doi-asserted-by":"publisher","first-page":"490","DOI":"10.1002\/adhm.201300311","volume":"3","author":"P Leleux","year":"2014","unstructured":"Leleux, P. et al. Conducting Polymer Electrodes for Electroencephalography. Adv. Healthc. Mater. \n                           3, 490\u2013493 (2014).","journal-title":"Adv. Healthc. Mater."},{"key":"14697_CR13","doi-asserted-by":"publisher","DOI":"10.1038\/ncomms2573","volume":"4","author":"D Khodagholy","year":"2013","unstructured":"Khodagholy, D. et al. In vivo recordings of brain activity using organic transistors. Nat. Commun. \n                           4, 1575 (2013).","journal-title":"Nat. Commun."},{"key":"14697_CR14","first-page":"803","volume":"2012","author":"NC Hogan","year":"2012","unstructured":"Hogan, N. C., Talei-Franzesi, G., Abudayyeh, O., Taberner, A. & Hunter, I. Low-cost, flexible polymer arrays for long-term neuronal culture. Conf. Proc\u2026. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. IEEE Eng. Med. Biol. Soc. Annu. Conf. \n                           2012, 803\u20136 (2012).","journal-title":"Conf. Proc\u2026. Annu. Int. Conf. IEEE Eng. Med. Biol. Soc. IEEE Eng. Med. Biol. Soc. Annu. Conf."},{"key":"14697_CR15","doi-asserted-by":"publisher","first-page":"3393","DOI":"10.1016\/j.biomaterials.2008.04.047","volume":"29","author":"RA Green","year":"2008","unstructured":"Green, R. A., Lovell, N. H., Wallace, G. G. & Poole-Warren, L. A. Conducting polymers for neural interfaces: Challenges in developing an effective long-term implant. Biomaterials \n                           29, 3393\u20133399 (2008).","journal-title":"Biomaterials"},{"key":"14697_CR16","doi-asserted-by":"publisher","first-page":"8","DOI":"10.3389\/fneng.2012.00008","volume":"5","author":"R Gerwig","year":"2012","unstructured":"Gerwig, R. et al. PEDOT\u2013CNT Composite Microelectrodes for Recording and Electrostimulation Applications: Fabrication, Morphology, and Electrical Properties. Front. Neuroeng. \n                           5, 8 (2012).","journal-title":"Front. Neuroeng."},{"key":"14697_CR17","doi-asserted-by":"crossref","unstructured":"Aregueta-Robles, U. A., Woolley, A. J., Poole-Warren, L. A., Lovell, N. H. & Green, R. A.Organic electrode coatings for next-generation neural interfaces. Front. Neuroeng. 7 (2014).","DOI":"10.3389\/fneng.2014.00015"},{"key":"14697_CR18","doi-asserted-by":"publisher","first-page":"6424","DOI":"10.1039\/C5TC00569H","volume":"3","author":"Y Fang","year":"2015","unstructured":"Fang, Y., Li, X. & Fang, Y. Organic bioelectronics for neural interfaces. J. Mater. Chem. C \n                           3, 6424\u20136430 (2015).","journal-title":"J. Mater. Chem. C"},{"key":"14697_CR19","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fneng.2011.00014","volume":"4","author":"A Fendyur","year":"2011","unstructured":"Fendyur, A., Mazurski, N., Shappir, J. & Spira, M. E. Formation of Essential Ultrastructural Interface between Cultured Hippocampal Cells and Gold Mushroom-Shaped MEA- Toward\u202f\u201cIN-CELL\u201d Recordings from Vertebrate Neurons. Front. Neuroeng. \n                           4, 1\u201314 (2011).","journal-title":"Front. Neuroeng."},{"key":"14697_CR20","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fneng.2012.00021","volume":"5","author":"A Fendyur","year":"2012","unstructured":"Fendyur, A. & Spira, M. E. Toward on-chip, in-cell recordings from cultured cardiomyocytes by arrays of gold mushroom-shaped microelectrodes. Front. Neuroeng. \n                           5, 1\u201310 (2012).","journal-title":"Front. Neuroeng."},{"key":"14697_CR21","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1523\/JNEUROSCI.07-01-00101.1987","volume":"7","author":"L Nowak","year":"1987","unstructured":"Nowak, L., Ascher, P. & Berwald-Netter, Y. Ionic channels in mouse astrocytes in culture. J. Neurosci. \n                           7, 101\u20139 (1987).","journal-title":"J. Neurosci."},{"key":"14697_CR22","doi-asserted-by":"publisher","first-page":"520","DOI":"10.1016\/j.tins.2003.08.006","volume":"26","author":"B Ransom","year":"2003","unstructured":"Ransom, B., Behar, T. & Nedergaard, M. New roles for astrocytes (stars at last). Trends Neurosci. \n                           26, 520\u2013522 (2003).","journal-title":"Trends Neurosci."},{"key":"14697_CR23","doi-asserted-by":"publisher","first-page":"300","DOI":"10.1016\/j.tcb.2016.01.003","volume":"26","author":"E Shigetomi","year":"2016","unstructured":"Shigetomi, E., Patel, S. & Khakh, B. S. Probing the Complexities of Astrocyte Calcium Signaling. Trends Cell Biol. \n                           26, 300\u2013312 (2016).","journal-title":"Trends Cell Biol."},{"key":"14697_CR24","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1038\/nn.4201","volume":"19","author":"N Bazargani","year":"2016","unstructured":"Bazargani, N. & Attwell, D. Astrocyte calcium signaling: the third wave. Nat. Neurosci. \n                           19, 182\u2013189 (2016).","journal-title":"Nat. Neurosci."},{"key":"14697_CR25","first-page":"7817","volume":"17","author":"L Pasti","year":"1997","unstructured":"Pasti, L., Volterra, A., Pozzan, T. & Carmignoto, G. Intracellular Calcium Oscillations in Astrocytes: A Highly Plastic, Astrocytes. In Situ. \n                           17, 7817\u20137830 (1997).","journal-title":"In Situ."},{"key":"14697_CR26","doi-asserted-by":"publisher","first-page":"2706","DOI":"10.1152\/jn.00509.2016","volume":"116","author":"E Wanke","year":"2016","unstructured":"Wanke, E., Gullo, F., Dossi, E., Valenza, G. & Becchetti, A. Neuron-glia cross talk revealed in reverberating networks by simultaneous extracellular recording of spikes and astrocytes\u2019 glutamate transporter and K+ currents. J. Neurophysiol. \n                           116, 2706\u20132719 (2016).","journal-title":"J. Neurophysiol."},{"key":"14697_CR27","doi-asserted-by":"publisher","first-page":"e12400","DOI":"10.14814\/phy2.12400","volume":"3","author":"W Fleischer","year":"2015","unstructured":"Fleischer, W., Theiss, S., Slotta, J., Holland, C. & Schnitzler, A. High-frequency voltage oscillations in cultured astrocytes. Physiol. Rep. \n                           3, e12400\u2013e12400 (2015).","journal-title":"Physiol. Rep."},{"key":"14697_CR28","doi-asserted-by":"publisher","first-page":"e1600516","DOI":"10.1126\/sciadv.1600516","volume":"2","author":"PRF Rocha","year":"2016","unstructured":"Rocha, P. R. F. et al. Extracellular electrical recording of pH-triggered bursts in C6 glioma cell populations. Sci. Adv. \n                           2, e1600516 (2016).","journal-title":"Sci. Adv."},{"key":"14697_CR29","doi-asserted-by":"publisher","first-page":"5035","DOI":"10.1039\/C5TB00144G","volume":"3","author":"PRF Rocha","year":"2015","unstructured":"Rocha, P. R. F. et al. Low frequency electric current noise in glioma cell populations. J. Mater. Chem. B \n                           3, 5035\u20135039 (2015).","journal-title":"J. Mater. Chem. B"},{"key":"14697_CR30","doi-asserted-by":"publisher","DOI":"10.1038\/srep34843","volume":"6","author":"PRF Rocha","year":"2016","unstructured":"Rocha, P. R. F. et al. Electrochemical noise and impedance of Au electrode\/electrolyte interfaces enabling extracellular detection of glioma cell populations. Sci. Rep. \n                           6, 34843 (2016).","journal-title":"Sci. Rep."},{"key":"14697_CR31","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.sbsr.2016.06.002","volume":"10","author":"MCR Medeiros","year":"2016","unstructured":"Medeiros, M. C. R. et al. An electrical method to measure low-frequency collective and synchronized cell activity using extracellular electrodes. Sens. Bio-Sensing Res. \n                           10, 1\u20138 (2016).","journal-title":"Sens. Bio-Sensing Res."},{"issue":"2","key":"14697_CR32","doi-asserted-by":"publisher","first-page":"252","DOI":"10.1109\/JPROC.2010.2066532","volume":"9","author":"BA Hierlemann","year":"2011","unstructured":"Hierlemann, B. A., Frey, U., Hafizovic, S. & Heer, F. Hierlemann. Growing Cells Atop Microelectronic Chips: Interfacing Electrogenic Cells In Vitro With CMOS-Based MicroelectrodeArrays. Proceeedings of the IEEE \n                           9(2), 252\u2013284 (2011).","journal-title":"Proceeedings of the IEEE"},{"key":"14697_CR33","doi-asserted-by":"crossref","unstructured":"Guo, J., Member, S., Yuan, J., Chan, M. & Member, S. Modeling of the Cell-Electrode Interface Noise for Microelectrode Arrays. 6, 605\u2013613 (2013).","DOI":"10.1109\/TBCAS.2012.2189569"},{"key":"14697_CR34","doi-asserted-by":"crossref","unstructured":"Inacio, P. M. C. et al. Bioelectrical Signal Detection Using Conducting Polymer Electrodes and the Displacement Current Method. IEEE Sens. J. 17 (2017).","DOI":"10.1109\/JSEN.2017.2703834"},{"key":"14697_CR35","doi-asserted-by":"publisher","first-page":"1074","DOI":"10.1063\/1.1755429","volume":"96","author":"A Hassibi","year":"2004","unstructured":"Hassibi, A., Navid, R., Dutton, R. W. & Lee, T. H. Comprehensive study of noise processes in electrode electrolyte interfaces. J. Appl. Phys. \n                           96, 1074\u20131082 (2004).","journal-title":"J. Appl. Phys."},{"key":"14697_CR36","doi-asserted-by":"publisher","DOI":"10.1038\/srep08876","volume":"5","author":"E Yamamoto","year":"2015","unstructured":"Yamamoto, E., Akimoto, T., Yasui, M. & Yasuoka, K. Origin of 1\/f noise in hydration dynamics on lipid membrane surfaces. Sci. Rep. \n                           5, 8876 (2015).","journal-title":"Sci. Rep."},{"key":"14697_CR37","doi-asserted-by":"publisher","first-page":"158101","DOI":"10.1103\/PhysRevLett.89.158101","volume":"89","author":"Z Siwy","year":"2002","unstructured":"Siwy, Z. & Fuli\u0144ski, A. Origin of 1\/f\u03b1 noise in membrane channel currents. Phys. Rev. Lett. \n                           89, 158101 (2002).","journal-title":"Phys. Rev. Lett."},{"key":"14697_CR38","doi-asserted-by":"publisher","first-page":"1295","DOI":"10.1109\/TBME.2005.847523","volume":"52","author":"W Franks","year":"2005","unstructured":"Franks, W., Schenker, I., Schmutz, P. & Hierlemann, A. Impedance Characterization and Modeling of Electrodes for Biomedical Applications. IEEE Trans. Biomed. Eng. \n                           52, 1295\u20131302 (2005).","journal-title":"IEEE Trans. Biomed. Eng."},{"key":"14697_CR39","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1002\/glia.440050203","volume":"5","author":"A Fatatis","year":"1992","unstructured":"Fatatis, A. & Russell, J. T. Spontaneous changes in intracellular calcium concentration in type I astrocytes from rat cerebral cortex in primary culture. Glia \n                           5, 95\u2013104 (1992).","journal-title":"Glia"},{"key":"14697_CR40","doi-asserted-by":"publisher","first-page":"2202","DOI":"10.1016\/j.bpj.2009.08.003","volume":"97","author":"SM Krug","year":"2009","unstructured":"Krug, S. M., Fromm, M. & G\u00fcnzel, D. Two-path impedance spectroscopy for measuring paracellular and transcellular epithelial resistance. Biophys. J. \n                           97, 2202\u20132211 (2009).","journal-title":"Biophys. J."},{"key":"14697_CR41","doi-asserted-by":"crossref","unstructured":"Tria, S. A., Ramuz, M., Jimison, L. H., Hama, A. & Owens, R. M. Sensing of Barrier Tissue Disruption with an Organic Electrochemical Transistor. 1\u20138 (2014).","DOI":"10.3791\/51102"},{"key":"14697_CR42","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1007\/s00232-001-0182-2","volume":"188","author":"B Rothen-Rutishauser","year":"2002","unstructured":"Rothen-Rutishauser, B., Riesen, F. K., Braun, A., G\u00fcnthert, M. & Wunderli-Allenspach, H. Dynamics of tight and adherens junctions under EGTA treatment. J. Membr. Biol. \n                           188, 151\u2013162 (2002).","journal-title":"J. Membr. Biol."},{"key":"14697_CR43","doi-asserted-by":"publisher","first-page":"3055","DOI":"10.1007\/s10439-011-0387-1","volume":"39","author":"V Savolainen","year":"2011","unstructured":"Savolainen, V. et al. Impedance spectroscopy in monitoring the maturation of stem cell-derived retinal pigment epithelium. Ann. Biomed. Eng. \n                           39, 3055\u20133069 (2011).","journal-title":"Ann. Biomed. Eng."},{"key":"14697_CR44","doi-asserted-by":"publisher","first-page":"3761","DOI":"10.1073\/pnas.81.12.3761","volume":"81","author":"I Giaever","year":"1984","unstructured":"Giaever, I. & Keese, C. R. Monitoring fibroblast behavior in tissue culture with an applied electric field. Proc. Natl. Acad. Sci. USA \n                           81, 3761\u20133764 (1984).","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"14697_CR45","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1085\/jgp.201210949","volume":"141","author":"E Shigetomi","year":"2013","unstructured":"Shigetomi, E. et al. Imaging calcium microdomains within entire astrocyte territories and endfeet with GCaMPs expressed using adeno-associated viruses. J. Gen. Physiol. \n                           141, 633\u2013647 (2013).","journal-title":"J. Gen. Physiol."},{"key":"14697_CR46","first-page":"95","volume":"104","author":"A Fatatis","year":"1992","unstructured":"Fatatis, A. & Russell, J. T. Spontaneous Changes in Intracellular Calcium Concentration in Type I Astrocytes From Rat Cerebral Cortex in Primary. Culture. \n                           104, 95\u2013104 (1992).","journal-title":"Culture."},{"key":"14697_CR47","doi-asserted-by":"publisher","first-page":"470","DOI":"10.1126\/science.1967852","volume":"247","author":"A Cornell-Bell","year":"1990","unstructured":"Cornell-Bell, A., Finkbeiner, S., Cooper, M. & Smith, S. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science (80-.). \n                           247, 470\u2013473 (1990).","journal-title":"Science (80-.)."},{"key":"14697_CR48","doi-asserted-by":"publisher","first-page":"2607","DOI":"10.1523\/JNEUROSCI.5319-10.2011","volume":"31","author":"N Kuga","year":"2011","unstructured":"Kuga, N., Sasaki, T., Takahara, Y., Matsuki, N. & Ikegaya, Y. Large-Scale Calcium Waves Traveling through Astrocytic Networks In Vivo. J. Neurosci. \n                           31, 2607\u20132614 (2011).","journal-title":"J. Neurosci."},{"key":"14697_CR49","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1093\/cercor\/bhj013","volume":"16","author":"R Zur Nieden","year":"2005","unstructured":"Zur Nieden, R. The Role of Metabotropic Glutamate Receptors for the Generation of Calcium Oscillations in Rat Hippocampal Astrocytes In Situ. Cereb. Cortex \n                           16, 676\u2013687 (2005).","journal-title":"Cereb. Cortex"},{"key":"14697_CR50","doi-asserted-by":"publisher","first-page":"708","DOI":"10.1038\/nn.4001","volume":"18","author":"R Srinivasan","year":"2015","unstructured":"Srinivasan, R. et al. Ca2+ signaling in astrocytes from Ip3r2\u2212\/\u2212 mice in brain slices and during startle responses in vivo. Nat. Neurosci. \n                           18, 708\u2013717 (2015).","journal-title":"Nat. Neurosci."},{"key":"14697_CR51","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1038\/nrd2552","volume":"7","author":"J Dunlop","year":"2008","unstructured":"Dunlop, J., Bowlby, M., Peri, R., Vasilyev, D. & Arias, R. High-throughput electrophysiology: an emerging paradigm for ion-channel screening and physiology. Nat. Rev. Drug Discov. \n                           7, 358\u2013368 (2008).","journal-title":"Nat. Rev. Drug Discov."},{"key":"14697_CR52","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fncel.2013.00159","volume":"7","author":"G Dall\u00e9rac","year":"2013","unstructured":"Dall\u00e9rac, G., Chever, O. & Rouach, N. How do astrocytes shape synaptic transmission? Insights from electrophysiology. Front. Cell. Neurosci. \n                           7, 1\u201319 (2013).","journal-title":"Front. Cell. Neurosci."},{"key":"14697_CR53","doi-asserted-by":"crossref","unstructured":"Stobart, J. L. & Anderson, C. M. Multifunctional role of astrocytes as gatekeepers of neuronal energy supply. Front. Cell. Neurosci. 7 (2013).","DOI":"10.3389\/fncel.2013.00038"},{"key":"14697_CR54","doi-asserted-by":"publisher","first-page":"13268","DOI":"10.1073\/pnas.93.23.13268","volume":"93","author":"TD Hassinger","year":"1996","unstructured":"Hassinger, T. D., Guthrie, P. B., Atkinson, P. B., Bennett, M. V. L. & Kater, S. B. An extracellular signaling component in propagation of astrocytic calcium waves. Proc. Natl. Acad. Sci. \n                           93, 13268\u201313273 (1996).","journal-title":"Proc. Natl. Acad. Sci."},{"key":"14697_CR55","doi-asserted-by":"crossref","first-page":"2782","DOI":"10.1152\/jn.1998.79.5.2782","volume":"79","author":"A Bordey","year":"1998","unstructured":"Bordey, A. & Sontheimer, H. Electrophysiological properties of human astrocytic tumor cells In situ: enigma of spiking glial cells. J. Neurophysiol. \n                           79, 2782\u201393 (1998).","journal-title":"J. Neurophysiol."},{"key":"14697_CR56","doi-asserted-by":"publisher","first-page":"979","DOI":"10.1016\/S0306-4522(03)00379-8","volume":"120","author":"H Parri","year":"2003","unstructured":"Parri, H. & Crunelli, V. The role of Ca2+ in the generation of spontaneous astrocytic Ca2+ oscillations. Neuroscience \n                           120, 979\u2013992 (2003).","journal-title":"Neuroscience"},{"key":"14697_CR57","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1016\/S0006-3495(01)75996-6","volume":"80","author":"T H\u00f6fer","year":"2001","unstructured":"H\u00f6fer, T., Politi, A. & Heinrich, R. Intercellular Ca2+ Wave Propagation through Gap-Junctional Ca2+ Diffusion: A Theoretical Study. Biophys. J. \n                           80, 75\u201387 (2001).","journal-title":"Biophys. J."},{"key":"14697_CR58","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1007\/s12015-009-9080-2","volume":"5","author":"S Sundelacruz","year":"2009","unstructured":"Sundelacruz, S., Levin, M. & Kaplan, D. L. Role of Membrane Potential in the Regulation of Cell Proliferation and Differentiation. Stem Cell Rev. Reports \n                           5, 231\u2013246 (2009).","journal-title":"Stem Cell Rev. Reports"},{"key":"14697_CR59","doi-asserted-by":"publisher","first-page":"14","DOI":"10.1016\/j.biosystems.2014.10.006","volume":"127","author":"DE Friesen","year":"2015","unstructured":"Friesen, D. E., Craddock, T. J. A., Kalra, A. P. & Tuszynski, J. A. Biological wires, communication systems, and implications for disease. Biosystems \n                           127, 14\u201327 (2015).","journal-title":"Biosystems"},{"key":"14697_CR60","doi-asserted-by":"publisher","first-page":"343","DOI":"10.3389\/fncel.2014.00343","volume":"8","author":"BP Carreira","year":"2014","unstructured":"Carreira, B. P. et al. Nitric oxide from inflammatory origin impairs neural stem cell proliferation by inhibiting epidermal growth factor receptor signaling. Front. Cell. Neurosci. \n                           8, 343 (2014).","journal-title":"Front. Cell. Neurosci."}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-14697-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-14697-y","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-14697-y.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,23]],"date-time":"2022-12-23T12:43:24Z","timestamp":1671799404000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-017-14697-y"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,10,27]]},"references-count":60,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2017,12]]}},"alternative-id":["14697"],"URL":"https:\/\/doi.org\/10.1038\/s41598-017-14697-y","relation":{},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,10,27]]},"assertion":[{"value":"31 May 2017","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"17 October 2017","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"27 October 2017","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare that they have no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"14284"}}