Formation of essential ultrastructural interface between cultured hippocampal cells and gold mushroom-shaped MEA- towards "IN-CELL" recordings from vertebrate neurons

A. Fendyur; N. Mazurski; J. Shappir; M.E. Spira

doi:10.3389/fneng.2011.00014

Formation of essential ultrastructural interface between cultured hippocampal cells and gold mushroom-shaped MEA- towards "IN-CELL" recordings from vertebrate neurons

A. Fendyur, N. Mazurski, J. Shappir, M.E. Spira

Institute for Medical Research Israel-Canada (IMRIC)

Research output: Contribution to journal › Article › peer-review

39 Scopus citations

Abstract

Using cultured Aplysia neurons we recently reported on the development of a novel approach in which an extracellular, noninvasive multi-electrode-array system provides multisite, attenuated, intracellular recordings of sub-threshold synaptic potentials and action potentials (APs), the so called "IN-CELL" recording configuration. Because of its noninvasive nature, the configuration can be used for long term semi intracellular electrophysiological monitoring of APs and synaptic potentials. Three principals converge to generate the IN-CELL configuration: (a) engulfment of approximately one micrometer size gold mushroom-shaped microelectrodes (gMμE) by the neurons, (b) formation of high seal resistance between the cell's plasma membrane and the engulfed gMμE and (c), autonomous localized increased conductance of the membrane patch facing the gMμE. Using dissociated rat hippocampal cultures we report here that the necessary morphological and ultrastructural relationships to generate the IN-CELL recording configuration are formed between hippocampal cells and the gMμEs. Interestingly, even

Original language	English
Journal	Frontiers in Neuroengineering
Issue number	NOVEMBER
DOIs	https://doi.org/10.3389/fneng.2011.00014
State	Published - 2011

Bibliographical note

Cited By :38

Export Date: 11 September 2022

Correspondence Address: Spira, M. E.; Department of Neurobiology, , Jerusalem, 91940, Israel; email: Spira@cc.huji.ac.il

References: Akaike, N., Harata, N., Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms (1994) Jpn J Physiol,, 44, pp. 433-473; Ambros-Ingerson, J., Holmes, W.R., Analysis and comparison of morphological reconstructions of hippocampal field CA1 pyramidal cells (2005) Hippocampus,, 15, pp. 302-315; Berdondini, L., Massobrio, P., Chiappalone, M., Tedesco, M., Imfeld, K., McCione, A., Gandolfo, M., Martinoia, S., Extracellular recordings from locally dense microelectrode arrays coupled to dissociated cortical cultures (2009) J Neurosci Methods,, 177, pp. 386-396; Claverol-Tinture, E., Pine, J., Extracellular potentials in low-density dissociated neuronal cultures (2002) J Neurosci Meth, 117, pp. 13-21; Cohen, A., Shappir, J., Yitzchaik, S., Spira, M.E., Reversible transition of extracellular field potential recordings to intracellular recordings of action potentials generated by neurons grown on transistors (2008) Biosens Bioelectron,, 23, pp. 811-819; Craig, A.M., Banker, G., Neuronal polarity (1994) Annu Rev Neurosci,, 17, pp. 267-310; Einevoll, G.T., Wojcik, D.K., Destexhe, A., Modeling extracellular potentials (2010) J Comput Neurosci,, 29, pp. 367-369; Fromherz, P., (2003) Neuroelectronic interfacing: Semiconductor chips with ion channels, nerve cells, and brain., , Berlin: Wiley-VCH; Fromherz, P., Three levels of neuroelectronic interfacing: Silicon chips with ion channels, nerve cells, and brain tissue (2006) Ann N Y Acad Sci,, 1093, pp. 143-160; Gitler, D., Xu, Y., Kao, H.T., Lin, D., Lim, S., Feng, J., Greengard, P., Augustine, G.J., Molecular determinants of synapsin targeting to presynaptic terminals (2004) J Neurosci,, 24, pp. 3711-3720; Hai, A., Dormann, A., Shappir, J., Yitzchaik, S., Bartic, C., Borghs, G., Langedijk, J.P., Spira, M.E., Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices (2009) J R Soc Interface,, 6, pp. 1153-1165; Hai, A., Kamber, D., Malkinson, G., Erez, H., Mazurski, N., Shappir, J., Spira, M.E., Changing gears from chemical adhesion of cells to flat substrata toward engulfment of micro-protrusions by active mechanisms (2009) J Neural Eng,, 6, p. 066009; Hai, A., Shappir, J., Spira, M.E., In-cell recordings by extracellular microelectrodes (2010) Nat Methods,, 7, pp. 200-202; Hai, A., Shappir, J., Spira, M.E., Long-term, multisite, parallel, in-cell recording and stimulation by an array of extracellular microelectrodes (2010) J Neurophysiol,, 104, pp. 559-568; Halassa, M.M., Haydon, P.G., Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior (2010) Annu Rev Physiol,, 72, pp. 335-355; Hochberg, L.R., Serruya, M.D., Friehs, G.M., Mukand, J.A., Saleh, M., Caplan, A.H., Branner, A., Donoghue, J.P., Neuronal ensemble control of prosthetic devices by a human with tetraplegia (2006) Nature,, 442, pp. 164-171; Inyushin, M., Tsytsarev, V., Ignashchenkova, A., Lenkov, D.N., Use of artificial ion channels for quasi-intracellular recording of cerebral cortex neuron activity (1997) Neurosci Behav Physiol,, 27, pp. 702-707; Jenkner, M., Fromherz, P., Bistability of membrane conductance in cell adhesion observed in a neuron transistor (1997) Phys. Rev. Lett.,, 79, pp. 4705-4708; Johnstone, A.F., Gross, G.W., Weiss, D.G., Schroeder, O.H., Gramowski, A., Shafer, T.J., Microelectrode arrays: A physiologically based neurotoxicity testing platform for the 21st century (2010) Neurotoxicology,, 31, pp. 331-350; Lebedev, M.A., Nicolelis, M.A., Brain-machine interfaces: Past, present and future (2006) Trends Neurosci,, 29, pp. 536-546; Linden, D.J., Long-term potentiation of glial synaptic currents in cerebellar culture (1997) Neuron,, 18, pp. 983-994; McCione, A., Gandolfo, M., Tedesco, M., Nieus, T., Imfeld, K., Martinoia, S., Berdondini, L., Experimental Investigation on Spontaneously Active Hippocampal Cultures Recorded by Means of High-Density MEAs: Analysis of the Spatial Resolution Effects (2010) Front Neuroeng,, 10, pp. 3-4; Markram, H., Perin, R., Innate neural assemblies for lego memory (2011) Front Neural Circuits,, 5, p. 6; McAdams, E.T., Jossinet, J., Subramanian, R., McCauley, R.G., Characterization of gold electrodes in phosphate buffered saline solution by impedance and noise measurements for biological applications (2006) Conf Proc IEEE Eng Med Biol Soc,, 1, pp. 4594-4597; McMahon, H.T., Gallop, J.L., Membrane curvature and mechanisms of dynamic cell membrane remodelling (2005) Nature,, 438, pp. 590-596; Mennerick, S., Benz, A., Zorumski, C.F., Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures (1996) J Neurosci,, 16, pp. 55-64; Mennerick, S., Zorumski, C.F., Glial contributions to excitatory neurotransmission in cultured hippocampal cells (1994) Nature,, 368, pp. 59-62; Mirsky, V.M., Riepl, M., Wolfbeis, O.S., Capacitive monitoring of protein immobilization and antigen-antibody reactions on monomolecular alkylthiol films on gold electrodes (1997) Biosens Bioelectron,, 12, pp. 977-989; Murphy, T.H., Blatter, L.A., Wier, W.G., Baraban, J.M., Rapid communication between neurons and astrocytes in primary cortical cultures (1993) J Neurosci,, 13, pp. 2672-2679; Nam, Y., Branch, D.W., Wheeler, B.C., Epoxy-silane linking of biomolecules is simple and effective for patterning neuronal cultures (2006) Biosens Bioelectron,, 22, pp. 589-597; Orkand, R.K., Nicholls, J.G., Kuffler, S.W., Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia (1966) J Neurophysiol,, 29, pp. 788-806; Perin, R., Berger, T.K., Markram, H., A synaptic organizing principle for cortical neuronal groups (2011) Proc Natl Acad Sci,, 108, pp. 5419-5424; Quiroga, R.Q., Nadasdy, Z., Ben-Shaul, Y., Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering (2004) Neural Comput,, 16, pp. 1661-1687; Rothman, S., Cowan, W.M., A scanning electron microscope study of the in vitro development of dissociated hippocampal cells (1981) J Comp Neurol,, 195, pp. 141-155; Sakmann, B., Neher, E., Patch clamp techniques for studying ionic channels in excitable membranes (1984) Annu Rev Physiol,, 46, pp. 455-472; Schipke, C.G., Kettenmann, H., Astrocyte responses to neuronal activity (2004) Glia,, 47, pp. 226-232; Scorza, C.A., Araujo, B.H., Leite, L.A., Torres, L.B., Otalora, L.F., Oliveira, M.S., Garrido-Sanabria, E.R., Cavalheiro, E.A., Morphological and electrophysiological properties of pyramidal-like neurons in the stratum oriens of Cornu ammonis 1 and Cornu ammonis 2 area of Proechimys (2011) Neuroscience,, 177, pp. 252-268; Soussou, W.V., Yoon, G.J., Brinton, R.D., Berger, T.W., Neuronal network morphology and electrophysiologyof hippocampal neurons cultured on surface-treated multielectrode arrays (2007) IEEE Trans Biomed Eng,, 54, pp. 1309-1320; Spira, M.E., Kamber, D., Dormann, A., Cohen, A., Bartic, C., Borghs, G., Langedijk, J.P.M., Shappir, J., Improved neuronal adhesion to the surface of electronic device by engulfment of protruding micro-nails fabricated on the chip surface (2007) Transducers '07 & Eurosensors Xxi Digest of Technical Papers, 1-2, pp. U628; Spira, M.E., Oren, R., Dormann, A., Gitler, D., Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons (2003) J Comp Neurol,, 457, pp. 293-312; Spruston, N., Johnston, D., Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons (1992) J Neurophysiol,, 67, pp. 508-529; Studer, D., Humbel, B.M., Chiquet, M., Electron microscopy of high pressure frozen samples: Bridging the gap between cellular ultrastructure and atomic resolution (2008) Histochem Cell Biol,, 130, pp. 877-889; Velez-Fort, M., Audinat, E., Angulo, M.C., Central Role of GABA in Neuron-Glia Interactions (2011) Neuroscientist.; Wheeler, B.C., Nam, Y., In vitro microelectrode array technology and neural recordings (2011) Crit Rev Biomed Eng,, 39, pp. 45-61

Keywords

Action potential
Electrical coupling
Field potentials
Gold mushroom-shaped microelectrodes
MEA
Multi-electrode-array
animal cell
article
brain computer interface
cell activity
cell membrane
cell structure
controlled study
electroencephalogram
gold mushroom shape microelectrode
hippocampus
information processing
intracellular recording
microelectrode
nerve cell
nerve potential
nervous system conductance
nervous system electrophysiology
newborn
nonhuman
rat
synaptic potential

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10.3389/fneng.2011.00014

https://www.scopus.com/inward/record.uri?eid=2-s2.0-84855478844&doi=10.3389%2ffneng.2011.00014&partnerID=40&md5=122b8f4455207dc195aefa4ca5b20ce4

Cite this

@article{31814e160b2e41daaa1306a8497e58d3,

title = "Formation of essential ultrastructural interface between cultured hippocampal cells and gold mushroom-shaped MEA- towards {"}IN-CELL{"} recordings from vertebrate neurons",

abstract = "Using cultured Aplysia neurons we recently reported on the development of a novel approach in which an extracellular, noninvasive multi-electrode-array system provides multisite, attenuated, intracellular recordings of sub-threshold synaptic potentials and action potentials (APs), the so called {"}IN-CELL{"} recording configuration. Because of its noninvasive nature, the configuration can be used for long term semi intracellular electrophysiological monitoring of APs and synaptic potentials. Three principals converge to generate the IN-CELL configuration: (a) engulfment of approximately one micrometer size gold mushroom-shaped microelectrodes (gMμE) by the neurons, (b) formation of high seal resistance between the cell's plasma membrane and the engulfed gMμE and (c), autonomous localized increased conductance of the membrane patch facing the gMμE. Using dissociated rat hippocampal cultures we report here that the necessary morphological and ultrastructural relationships to generate the IN-CELL recording configuration are formed between hippocampal cells and the gMμEs. Interestingly, even ",

keywords = "Action potential, Electrical coupling, Field potentials, Gold mushroom-shaped microelectrodes, MEA, Multi-electrode-array, animal cell, article, brain computer interface, cell activity, cell membrane, cell structure, controlled study, electroencephalogram, gold mushroom shape microelectrode, hippocampus, information processing, intracellular recording, microelectrode, nerve cell, nerve potential, nervous system conductance, nervous system electrophysiology, newborn, nonhuman, rat, synaptic potential",

author = "A. Fendyur and N. Mazurski and J. Shappir and M.E. Spira",

note = "Cited By :38 Export Date: 11 September 2022 Correspondence Address: Spira, M. E.; Department of Neurobiology, , Jerusalem, 91940, Israel; email: Spira@cc.huji.ac.il References: Akaike, N., Harata, N., Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms (1994) Jpn J Physiol,, 44, pp. 433-473; Ambros-Ingerson, J., Holmes, W.R., Analysis and comparison of morphological reconstructions of hippocampal field CA1 pyramidal cells (2005) Hippocampus,, 15, pp. 302-315; Berdondini, L., Massobrio, P., Chiappalone, M., Tedesco, M., Imfeld, K., McCione, A., Gandolfo, M., Martinoia, S., Extracellular recordings from locally dense microelectrode arrays coupled to dissociated cortical cultures (2009) J Neurosci Methods,, 177, pp. 386-396; Claverol-Tinture, E., Pine, J., Extracellular potentials in low-density dissociated neuronal cultures (2002) J Neurosci Meth, 117, pp. 13-21; Cohen, A., Shappir, J., Yitzchaik, S., Spira, M.E., Reversible transition of extracellular field potential recordings to intracellular recordings of action potentials generated by neurons grown on transistors (2008) Biosens Bioelectron,, 23, pp. 811-819; Craig, A.M., Banker, G., Neuronal polarity (1994) Annu Rev Neurosci,, 17, pp. 267-310; Einevoll, G.T., Wojcik, D.K., Destexhe, A., Modeling extracellular potentials (2010) J Comput Neurosci,, 29, pp. 367-369; Fromherz, P., (2003) Neuroelectronic interfacing: Semiconductor chips with ion channels, nerve cells, and brain., , Berlin: Wiley-VCH; Fromherz, P., Three levels of neuroelectronic interfacing: Silicon chips with ion channels, nerve cells, and brain tissue (2006) Ann N Y Acad Sci,, 1093, pp. 143-160; Gitler, D., Xu, Y., Kao, H.T., Lin, D., Lim, S., Feng, J., Greengard, P., Augustine, G.J., Molecular determinants of synapsin targeting to presynaptic terminals (2004) J Neurosci,, 24, pp. 3711-3720; Hai, A., Dormann, A., Shappir, J., Yitzchaik, S., Bartic, C., Borghs, G., Langedijk, J.P., Spira, M.E., Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices (2009) J R Soc Interface,, 6, pp. 1153-1165; Hai, A., Kamber, D., Malkinson, G., Erez, H., Mazurski, N., Shappir, J., Spira, M.E., Changing gears from chemical adhesion of cells to flat substrata toward engulfment of micro-protrusions by active mechanisms (2009) J Neural Eng,, 6, p. 066009; Hai, A., Shappir, J., Spira, M.E., In-cell recordings by extracellular microelectrodes (2010) Nat Methods,, 7, pp. 200-202; Hai, A., Shappir, J., Spira, M.E., Long-term, multisite, parallel, in-cell recording and stimulation by an array of extracellular microelectrodes (2010) J Neurophysiol,, 104, pp. 559-568; Halassa, M.M., Haydon, P.G., Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior (2010) Annu Rev Physiol,, 72, pp. 335-355; Hochberg, L.R., Serruya, M.D., Friehs, G.M., Mukand, J.A., Saleh, M., Caplan, A.H., Branner, A., Donoghue, J.P., Neuronal ensemble control of prosthetic devices by a human with tetraplegia (2006) Nature,, 442, pp. 164-171; Inyushin, M., Tsytsarev, V., Ignashchenkova, A., Lenkov, D.N., Use of artificial ion channels for quasi-intracellular recording of cerebral cortex neuron activity (1997) Neurosci Behav Physiol,, 27, pp. 702-707; Jenkner, M., Fromherz, P., Bistability of membrane conductance in cell adhesion observed in a neuron transistor (1997) Phys. Rev. Lett.,, 79, pp. 4705-4708; Johnstone, A.F., Gross, G.W., Weiss, D.G., Schroeder, O.H., Gramowski, A., Shafer, T.J., Microelectrode arrays: A physiologically based neurotoxicity testing platform for the 21st century (2010) Neurotoxicology,, 31, pp. 331-350; Lebedev, M.A., Nicolelis, M.A., Brain-machine interfaces: Past, present and future (2006) Trends Neurosci,, 29, pp. 536-546; Linden, D.J., Long-term potentiation of glial synaptic currents in cerebellar culture (1997) Neuron,, 18, pp. 983-994; McCione, A., Gandolfo, M., Tedesco, M., Nieus, T., Imfeld, K., Martinoia, S., Berdondini, L., Experimental Investigation on Spontaneously Active Hippocampal Cultures Recorded by Means of High-Density MEAs: Analysis of the Spatial Resolution Effects (2010) Front Neuroeng,, 10, pp. 3-4; Markram, H., Perin, R., Innate neural assemblies for lego memory (2011) Front Neural Circuits,, 5, p. 6; McAdams, E.T., Jossinet, J., Subramanian, R., McCauley, R.G., Characterization of gold electrodes in phosphate buffered saline solution by impedance and noise measurements for biological applications (2006) Conf Proc IEEE Eng Med Biol Soc,, 1, pp. 4594-4597; McMahon, H.T., Gallop, J.L., Membrane curvature and mechanisms of dynamic cell membrane remodelling (2005) Nature,, 438, pp. 590-596; Mennerick, S., Benz, A., Zorumski, C.F., Components of glial responses to exogenous and synaptic glutamate in rat hippocampal microcultures (1996) J Neurosci,, 16, pp. 55-64; Mennerick, S., Zorumski, C.F., Glial contributions to excitatory neurotransmission in cultured hippocampal cells (1994) Nature,, 368, pp. 59-62; Mirsky, V.M., Riepl, M., Wolfbeis, O.S., Capacitive monitoring of protein immobilization and antigen-antibody reactions on monomolecular alkylthiol films on gold electrodes (1997) Biosens Bioelectron,, 12, pp. 977-989; Murphy, T.H., Blatter, L.A., Wier, W.G., Baraban, J.M., Rapid communication between neurons and astrocytes in primary cortical cultures (1993) J Neurosci,, 13, pp. 2672-2679; Nam, Y., Branch, D.W., Wheeler, B.C., Epoxy-silane linking of biomolecules is simple and effective for patterning neuronal cultures (2006) Biosens Bioelectron,, 22, pp. 589-597; Orkand, R.K., Nicholls, J.G., Kuffler, S.W., Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia (1966) J Neurophysiol,, 29, pp. 788-806; Perin, R., Berger, T.K., Markram, H., A synaptic organizing principle for cortical neuronal groups (2011) Proc Natl Acad Sci,, 108, pp. 5419-5424; Quiroga, R.Q., Nadasdy, Z., Ben-Shaul, Y., Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering (2004) Neural Comput,, 16, pp. 1661-1687; Rothman, S., Cowan, W.M., A scanning electron microscope study of the in vitro development of dissociated hippocampal cells (1981) J Comp Neurol,, 195, pp. 141-155; Sakmann, B., Neher, E., Patch clamp techniques for studying ionic channels in excitable membranes (1984) Annu Rev Physiol,, 46, pp. 455-472; Schipke, C.G., Kettenmann, H., Astrocyte responses to neuronal activity (2004) Glia,, 47, pp. 226-232; Scorza, C.A., Araujo, B.H., Leite, L.A., Torres, L.B., Otalora, L.F., Oliveira, M.S., Garrido-Sanabria, E.R., Cavalheiro, E.A., Morphological and electrophysiological properties of pyramidal-like neurons in the stratum oriens of Cornu ammonis 1 and Cornu ammonis 2 area of Proechimys (2011) Neuroscience,, 177, pp. 252-268; Soussou, W.V., Yoon, G.J., Brinton, R.D., Berger, T.W., Neuronal network morphology and electrophysiologyof hippocampal neurons cultured on surface-treated multielectrode arrays (2007) IEEE Trans Biomed Eng,, 54, pp. 1309-1320; Spira, M.E., Kamber, D., Dormann, A., Cohen, A., Bartic, C., Borghs, G., Langedijk, J.P.M., Shappir, J., Improved neuronal adhesion to the surface of electronic device by engulfment of protruding micro-nails fabricated on the chip surface (2007) Transducers '07 & Eurosensors Xxi Digest of Technical Papers, 1-2, pp. U628; Spira, M.E., Oren, R., Dormann, A., Gitler, D., Critical calpain-dependent ultrastructural alterations underlie the transformation of an axonal segment into a growth cone after axotomy of cultured Aplysia neurons (2003) J Comp Neurol,, 457, pp. 293-312; Spruston, N., Johnston, D., Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons (1992) J Neurophysiol,, 67, pp. 508-529; Studer, D., Humbel, B.M., Chiquet, M., Electron microscopy of high pressure frozen samples: Bridging the gap between cellular ultrastructure and atomic resolution (2008) Histochem Cell Biol,, 130, pp. 877-889; Velez-Fort, M., Audinat, E., Angulo, M.C., Central Role of GABA in Neuron-Glia Interactions (2011) Neuroscientist.; Wheeler, B.C., Nam, Y., In vitro microelectrode array technology and neural recordings (2011) Crit Rev Biomed Eng,, 39, pp. 45-61",

year = "2011",

doi = "10.3389/fneng.2011.00014",

language = "אנגלית",

journal = "Frontiers in Neuroengineering",

issn = "1662-6443",

publisher = "Frontiers Media S.A.",

number = "NOVEMBER",

}

TY - JOUR

T1 - Formation of essential ultrastructural interface between cultured hippocampal cells and gold mushroom-shaped MEA- towards "IN-CELL" recordings from vertebrate neurons

AU - Fendyur, A.

AU - Mazurski, N.

AU - Shappir, J.

AU - Spira, M.E.

N1 - Cited By :38 Export Date: 11 September 2022 Correspondence Address: Spira, M. E.; Department of Neurobiology, , Jerusalem, 91940, Israel; email: Spira@cc.huji.ac.il References: Akaike, N., Harata, N., Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms (1994) Jpn J Physiol,, 44, pp. 433-473; Ambros-Ingerson, J., Holmes, W.R., Analysis and comparison of morphological reconstructions of hippocampal field CA1 pyramidal cells (2005) Hippocampus,, 15, pp. 302-315; Berdondini, L., Massobrio, P., Chiappalone, M., Tedesco, M., Imfeld, K., McCione, A., Gandolfo, M., Martinoia, S., Extracellular recordings from locally dense microelectrode arrays coupled to dissociated cortical cultures (2009) J Neurosci Methods,, 177, pp. 386-396; Claverol-Tinture, E., Pine, J., Extracellular potentials in low-density dissociated neuronal cultures (2002) J Neurosci Meth, 117, pp. 13-21; Cohen, A., Shappir, J., Yitzchaik, S., Spira, M.E., Reversible transition of extracellular field potential recordings to intracellular recordings of action potentials generated by neurons grown on transistors (2008) Biosens Bioelectron,, 23, pp. 811-819; Craig, A.M., Banker, G., Neuronal polarity (1994) Annu Rev Neurosci,, 17, pp. 267-310; Einevoll, G.T., Wojcik, D.K., Destexhe, A., Modeling extracellular potentials (2010) J Comput Neurosci,, 29, pp. 367-369; Fromherz, P., (2003) Neuroelectronic interfacing: Semiconductor chips with ion channels, nerve cells, and brain., , Berlin: Wiley-VCH; Fromherz, P., Three levels of neuroelectronic interfacing: Silicon chips with ion channels, nerve cells, and brain tissue (2006) Ann N Y Acad Sci,, 1093, pp. 143-160; Gitler, D., Xu, Y., Kao, H.T., Lin, D., Lim, S., Feng, J., Greengard, P., Augustine, G.J., Molecular determinants of synapsin targeting to presynaptic terminals (2004) J Neurosci,, 24, pp. 3711-3720; Hai, A., Dormann, A., Shappir, J., Yitzchaik, S., Bartic, C., Borghs, G., Langedijk, J.P., Spira, M.E., Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices (2009) J R Soc Interface,, 6, pp. 1153-1165; Hai, A., Kamber, D., Malkinson, G., Erez, H., Mazurski, N., Shappir, J., Spira, M.E., Changing gears from chemical adhesion of cells to flat substrata toward engulfment of micro-protrusions by active mechanisms (2009) J Neural Eng,, 6, p. 066009; Hai, A., Shappir, J., Spira, M.E., In-cell recordings by extracellular microelectrodes (2010) Nat Methods,, 7, pp. 200-202; Hai, A., Shappir, J., Spira, M.E., Long-term, multisite, parallel, in-cell recording and stimulation by an array of extracellular microelectrodes (2010) J Neurophysiol,, 104, pp. 559-568; Halassa, M.M., Haydon, P.G., Integrated brain circuits: Astrocytic networks modulate neuronal activity and behavior (2010) Annu Rev Physiol,, 72, pp. 335-355; Hochberg, L.R., Serruya, M.D., Friehs, G.M., Mukand, J.A., Saleh, M., Caplan, A.H., Branner, A., Donoghue, J.P., Neuronal ensemble control of prosthetic devices by a human with tetraplegia (2006) Nature,, 442, pp. 164-171; Inyushin, M., Tsytsarev, V., Ignashchenkova, A., Lenkov, D.N., Use of artificial ion channels for quasi-intracellular recording of cerebral cortex neuron activity (1997) Neurosci Behav Physiol,, 27, pp. 702-707; Jenkner, M., Fromherz, P., Bistability of membrane conductance in cell adhesion observed in a neuron transistor (1997) Phys. Rev. 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PY - 2011

Y1 - 2011

N2 - Using cultured Aplysia neurons we recently reported on the development of a novel approach in which an extracellular, noninvasive multi-electrode-array system provides multisite, attenuated, intracellular recordings of sub-threshold synaptic potentials and action potentials (APs), the so called "IN-CELL" recording configuration. Because of its noninvasive nature, the configuration can be used for long term semi intracellular electrophysiological monitoring of APs and synaptic potentials. Three principals converge to generate the IN-CELL configuration: (a) engulfment of approximately one micrometer size gold mushroom-shaped microelectrodes (gMμE) by the neurons, (b) formation of high seal resistance between the cell's plasma membrane and the engulfed gMμE and (c), autonomous localized increased conductance of the membrane patch facing the gMμE. Using dissociated rat hippocampal cultures we report here that the necessary morphological and ultrastructural relationships to generate the IN-CELL recording configuration are formed between hippocampal cells and the gMμEs. Interestingly, even

AB - Using cultured Aplysia neurons we recently reported on the development of a novel approach in which an extracellular, noninvasive multi-electrode-array system provides multisite, attenuated, intracellular recordings of sub-threshold synaptic potentials and action potentials (APs), the so called "IN-CELL" recording configuration. Because of its noninvasive nature, the configuration can be used for long term semi intracellular electrophysiological monitoring of APs and synaptic potentials. Three principals converge to generate the IN-CELL configuration: (a) engulfment of approximately one micrometer size gold mushroom-shaped microelectrodes (gMμE) by the neurons, (b) formation of high seal resistance between the cell's plasma membrane and the engulfed gMμE and (c), autonomous localized increased conductance of the membrane patch facing the gMμE. Using dissociated rat hippocampal cultures we report here that the necessary morphological and ultrastructural relationships to generate the IN-CELL recording configuration are formed between hippocampal cells and the gMμEs. Interestingly, even

KW - Action potential

KW - Electrical coupling

KW - Field potentials

KW - Gold mushroom-shaped microelectrodes

KW - MEA

KW - Multi-electrode-array

KW - animal cell

KW - article

KW - brain computer interface

KW - cell activity

KW - cell membrane

KW - cell structure

KW - controlled study

KW - electroencephalogram

KW - gold mushroom shape microelectrode

KW - hippocampus

KW - information processing

KW - intracellular recording

KW - microelectrode

KW - nerve cell

KW - nerve potential

KW - nervous system conductance

KW - nervous system electrophysiology

KW - newborn

KW - nonhuman

KW - rat

KW - synaptic potential

UR - http://www.scopus.com/inward/record.url?scp=84855478844&partnerID=8YFLogxK

U2 - 10.3389/fneng.2011.00014

DO - 10.3389/fneng.2011.00014

M3 - ???researchoutput.researchoutputtypes.contributiontojournal.article???

SN - 1662-6443

JO - Frontiers in Neuroengineering

JF - Frontiers in Neuroengineering

IS - NOVEMBER

ER -

Formation of essential ultrastructural interface between cultured hippocampal cells and gold mushroom-shaped MEA- towards "IN-CELL" recordings from vertebrate neurons

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