Multi-electrode array technologies for neuroscience and cardiology.

At present, the prime methodology for studying neuronal circuit-connectivity, physiology and pathology under in vitro or in vivo conditions is by using substrate-integrated microelectrode arrays. Although this methodology permits simultaneous, cell-non-invasive, long-term recordings of extracellular field potentials generated by action potentials, it is 'blind' to subthreshold synaptic potentials generated by single cells. On the other hand, intracellular recordings of the full electrophysiological repertoire (subthreshold synaptic potentials, membrane oscillations and action potentials) are, at present, obtained only by sharp or patch microelectrodes. These, however, are limited to single cells at a time and for short durations. Recently a number of laboratories began to merge the advantages of extracellular microelectrode arrays and intracellular microelectrodes. This Review describes the novel approaches, identifying their strengths and limitations from the point of view of the end users--with the intention to help steer the bioengineering efforts towards the needs of brain-circuit research.

[1]  I . THE DEVELOPMENT OR ELECTROPHYSIOLOGY , 1932 .

[2]  A. Hodgkin,et al.  Action Potentials Recorded from Inside a Nerve Fibre , 1939, Nature.

[3]  H. Grundfest.  The mechanisms of discharge of the electric organs in relation to general and comparative electrophysiology. , 1957, Progress in biophysics and biophysical chemistry.

[4]  G. Loeb,et al.  A miniature microelectrode array to monitor the bioelectric activity of cultured cells. , 1972, Experimental cell research.

[5]  J. Pine.  Recording action potentials from cultured neurons with extracellular microcircuit electrodes , 1980, Journal of Neuroscience Methods.

[6]  Guenter W. Gross,et al.  Recording of spontaneous activity with photoetched microelectrode surfaces from mouse spinal neurons in culture , 1982, Journal of Neuroscience Methods.

[7]  B Sakmann,et al.  Patch clamp techniques for studying ionic channels in excitable membranes. , 1984, Annual review of physiology.

[8]  F Bezanilla,et al.  Charge-shift probes of membrane potential. Characterization of aminostyrylpyridinium dyes on the squid giant axon. , 1985, Biophysical journal.

[9]  A.A. Abidi,et al.  High-frequency noise measurements on FET's with small dimensions , 1986, IEEE Transactions on Electron Devices.

[10]  T. Wiesel,et al.  Functional architecture of cortex revealed by optical imaging of intrinsic signals , 1986, Nature.

[11]  D. Senseman,et al.  Odor-elicited activity monitored simultaneously from 124 regions of the salamander olfactory bulb using a voltage-sensitive dye , 1987, Brain Research.

[12]  David W. Tank,et al.  Sealing cultured invertebrate neurons to embedded dish electrodes facilitates long-term stimulation and recording , 1989, Journal of Neuroscience Methods.

[13]  Matthew N. O. Sadiku,et al.  Elements of Electromagnetics , 1989 .

[14]  C. Wilkinson,et al.  An extracellular microelectrode array for monitoring electrogenic cells in culture. , 1990, Biosensors & bioelectronics.

[15]  N. Akaike,et al.  Nystatin perforated patch recording and its applications to analyses of intracellular mechanisms. , 1994, The Japanese journal of physiology.

[16]  Partha P. Mitra,et al.  Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability , 1996, Journal of Neuroscience Methods.

[17]  Ehud Y Isacoff,et al.  A Genetically Encoded Optical Probe of Membrane Voltage , 1997, Neuron.

[18]  P. Fromherz,et al.  Fluorescence interference-contrast microscopy of cell adhesion on oxidized silicon , 1997 .

[19]  A. Aderem,et al.  Mechanisms of phagocytosis in macrophages. , 1999, Annual review of immunology.

[20]  A. Grinvald,et al.  Imaging Cortical Dynamics at High Spatial and Temporal Resolution with Novel Blue Voltage-Sensitive Dyes , 1999, Neuron.

[21]  H. Oka,et al.  A new planar multielectrode array for extracellular recording: application to hippocampal acute slice , 1999, Journal of Neuroscience Methods.

[22]  J. Rizzo,et al.  Multi-electrode stimulation and recording in the isolated retina , 2000, Journal of Neuroscience Methods.

[23]  R. May,et al.  Phagocytosis and the actin cytoskeleton. , 2001, Journal of cell science.

[24]  P. Fromherz,et al.  No correlation of focal contacts and close adhesion by comparing GFP-vinculin and fluorescence interference of DiI , 2001, European Biophysics Journal.

[25]  E. Bamberg,et al.  Channelrhodopsin-1: A Light-Gated Proton Channel in Green Algae , 2002, Science.

[26]  Armin Lambacher,et al.  Luminescence of dye molecules on oxidized silicon and fluorescence interference contrast microscopy of biomembranes , 2002 .

[27]  W. Rutten.  Selective electrical interfaces with the nervous system. , 2002, Annual review of biomedical engineering.

[28]  P. Fromherz,et al.  Semiconductor chips with ion channels, nerve cells and brain slices , 2003, First International IEEE EMBS Conference on Neural Engineering, 2003. Conference Proceedings..

[29]  Enrico Marani,et al.  Geometry-based finite-element modeling of the electrical contact between a cultured neuron and a microelectrode , 2003, IEEE Transactions on Biomedical Engineering.

[30]  C. Stosiek,et al.  In vivo two-photon calcium imaging of neuronal networks , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[31]  N. Balaban,et al.  Adhesion-dependent cell mechanosensitivity. , 2003, Annual review of cell and developmental biology.

[32]  Peter Fromherz,et al.  Neuroelectronic Interfacing: Semiconductor Chips with Ion Channels, Nerve Cells, and Brain , 2012 .

[33]  R. Kass,et al.  Multiple neural spike train data analysis: state-of-the-art and future challenges , 2004, Nature Neuroscience.

[34]  Andrew B Schwartz,et al.  Cortical neural prosthetics. , 2004, Annual review of neuroscience.

[35]  Yasunori Hayashi,et al.  Dendritic Spine Geometry: Functional Implication and Regulation , 2005, Neuron.

[36]  Luke P. Lee,et al.  Mammalian electrophysiology on a microfluidic platform. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[37]  T. Blanche,et al.  Polytrodes: high-density silicon electrode arrays for large-scale multiunit recording. , 2005, Journal of neurophysiology.

[38]  Peter Fromherz,et al.  Nyquist noise of cell adhesion detected in a neuron-silicon transistor. , 2006, Physical review letters.

[39]  R. Segev,et al.  How silent is the brain: is there a “dark matter” problem in neuroscience? , 2006, Journal of Comparative Physiology A.

[40]  Luke P. Lee,et al.  Open-access microfluidic patch-clamp array with raised lateral cell trapping sites. , 2006, Lab on a chip.

[41]  Peter Fromherz,et al.  Three Levels of Neuroelectronic Interfacing , 2006, Annals of the New York Academy of Sciences.

[42]  Alexei Verkhratsky,et al.  From Galvani to patch clamp: the development of electrophysiology , 2006, Pflügers Archiv.

[43]  A. Lambacher,et al.  High-resolution multitransistor array recording of electrical field potentials in cultured brain slices. , 2006, Journal of neurophysiology.

[44]  Jon A. Mukand,et al.  Neuronal ensemble control of prosthetic devices by a human with tetraplegia , 2006, Nature.

[45]  Danny Eytan,et al.  Dynamics and Effective Topology Underlying Synchronization in Networks of Cortical Neurons , 2006, The Journal of Neuroscience.

[46]  P. Fromherz,et al.  The extracellular electrical resistivity in cell adhesion. , 2006, Biophysical journal.

[47]  J. Shappir,et al.  Improved Neuronal Adhesion to the Surface of Electronic Device by Engulfment of Protruding Micro-Nails Fabricated on the Chip Surface , 2007, TRANSDUCERS 2007 - 2007 International Solid-State Sensors, Actuators and Microsystems Conference.

[48]  Benjamin Geiger,et al.  Molecular engineering of cellular environments: cell adhesion to nano-digital surfaces. , 2007, Methods in cell biology.

[49]  Andreas Offenhäusser,et al.  Transmission electron microscopy study of the cell–sensor interface , 2008, Journal of The Royal Society Interface.

[50]  Shlomo Yitzchaik,et al.  Reversible transition of extracellular field potential recordings to intracellular recordings of action potentials generated by neurons grown on transistors. , 2008, Biosensors & bioelectronics.

[51]  B. Botterman,et al.  Carbon nanotube coating improves neuronal recordings. , 2008, Nature nanotechnology.

[52]  P. Fromherz,et al.  Extracellular stimulation of mammalian neurons through repetitive activation of Na+ channels by weak capacitive currents on a silicon chip. , 2008, Journal of neurophysiology.

[53]  B. Sabatini,et al.  Calcium Signaling in Dendrites and Spines: Practical and Functional Considerations , 2008, Neuron.

[54]  Carmen Bartic,et al.  Spine-shaped gold protrusions improve the adherence and electrical coupling of neurons with the surface of micro-electronic devices , 2009, Journal of The Royal Society Interface.

[55]  Charles M Lieber,et al.  Flexible electrical recording from cells using nanowire transistor arrays , 2009, Proceedings of the National Academy of Sciences.

[56]  Luca Berdondini,et al.  Active pixel sensor array for high spatio-temporal resolution electrophysiological recordings from single cell to large scale neuronal networks. , 2009, Lab on a chip.

[57]  H. McMahon,et al.  Mechanisms of endocytosis. , 2009, Annual review of biochemistry.

[58]  U. Frey,et al.  Microelectronic system for high-resolution mapping of extracellular electric fields applied to brain slices. , 2009, Biosensors & bioelectronics.

[59]  J. Shappir,et al.  Changing gears from chemical adhesion of cells to flat substrata toward engulfment of micro-protrusions by active mechanisms , 2009, Journal of neural engineering.

[60]  Bradley J. Baker,et al.  Wide-field and two-photon imaging of brain activity with voltage- and calcium-sensitive dyes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[61]  E. Ben-Jacob,et al.  Engineered neuronal circuits shaped and interfaced with carbon nanotube microelectrode arrays , 2009, Biomedical microdevices.

[62]  I. Nelken,et al.  Functional organization and population dynamics in the mouse primary auditory cortex , 2010, Nature Neuroscience.

[63]  Alberto Paleari,et al.  Glycine-Spacers Influence Functional Motifs Exposure and Self-Assembling Propensity of Functionalized Substrates Tailored for Neural Stem Cell Cultures , 2009, Front. Neuroeng..

[64]  J. Shappir,et al.  In-cell recordings by extracellular microelectrodes , 2010, Nature Methods.

[65]  J. Shappir,et al.  Long-term, multisite, parallel, in-cell recording and stimulation by an array of extracellular microelectrodes. , 2010, Journal of neurophysiology.

[66]  Yoonkey Nam,et al.  Surface-modified microelectrode array with flake nanostructure for neural recording and stimulation , 2010, Nanotechnology.

[67]  Wolfgang Eberle,et al.  A novel 16k micro-nail CMOS-chip for in-vitro single-cell recording, stimulation and impedance measurements , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[68]  G. Borghs,et al.  Single-cell stimulation and electroporation using a novel 0.18 µ CMOS chip with subcellular-sized electrodes , 2010, 2010 Annual International Conference of the IEEE Engineering in Medicine and Biology.

[69]  N. Melosh,et al.  Fusion of biomimetic stealth probes into lipid bilayer cores , 2010, Proceedings of the National Academy of Sciences.

[70]  Charles M. Lieber,et al.  Three-Dimensional, Flexible Nanoscale Field-Effect Transistors as Localized Bioprobes , 2010, Science.

[71]  Luca Berdondini,et al.  Experimental Investigation on Spontaneously Active Hippocampal Cultures Recorded by Means of High-Density MEAs: Analysis of the Spatial Resolution Effects , 2010, Front. Neuroeng..

[72]  Jacob G. Bernstein,et al.  Optogenetic tools for analyzing the neural circuits of behavior , 2011, Trends in Cognitive Sciences.

[73]  J. Shappir,et al.  Formation of Essential Ultrastructural Interface between Cultured Hippocampal Cells and Gold Mushroom-Shaped MEA- Toward “IN-CELL” Recordings from Vertebrate Neurons , 2011, Front. Neuroeng..

[74]  N. Melosh,et al.  Molecular structure influences the stability of membrane penetrating biointerfaces. , 2011, Nano letters.

[75]  M. Fiscella,et al.  The potential of microelectrode arrays and microelectronics for biomedical research and diagnostics , 2011, Analytical and bioanalytical chemistry.

[76]  Christophe Py,et al.  Recordings of cultured neurons and synaptic activity using patch-clamp chips , 2011, Journal of neural engineering.

[77]  Boris Hofmann,et al.  Nanocavity electrode array for recording from electrogenic cells. , 2011, Lab on a chip.

[78]  Bozhi Tian,et al.  Design, synthesis, and characterization of novel nanowire structures for photovoltaics and intracellular probes , 2011, Pure and applied chemistry. Chimie pure et appliquee.

[79]  Yoonkey Nam,et al.  In vitro microelectrode array technology and neural recordings. , 2011, Critical reviews in biomedical engineering.

[80]  B Wolfrum,et al.  Nanostructured gold microelectrodes for extracellular recording from electrogenic cells , 2011, Nanotechnology.

[81]  N. Melosh,et al.  Nanoscale patterning controls inorganic-membrane interface structure. , 2011, Nanoscale.

[82]  Bozhi Tian,et al.  Intracellular recordings of action potentials by an extracellular nanoscale field-effect transistor , 2011, Nature nanotechnology.

[83]  Eric R Kandel,et al.  Synapses and memory storage. , 2012, Cold Spring Harbor perspectives in biology.

[84]  Jacob T. Robinson,et al.  Vertical nanowire electrode arrays as a scalable platform for intracellular interfacing to neuronal circuits. , 2012, Nature nanotechnology.

[85]  Bozhi Tian,et al.  Outside looking in: nanotube transistor intracellular sensors. , 2012, Nano letters.

[86]  Jan Wouters,et al.  Single-cell recording and stimulation with a 16k micro-nail electrode array integrated on a 0.18 μm CMOS chip. , 2012, Lab on a chip.

[87]  B. Cui,et al.  Intracellular Recording of Action Potentials by Nanopillar Electroporation , 2012, Nature nanotechnology.

[88]  Nadine Collaert,et al.  Open-cell recording of action potentials using active electrode arrays. , 2012, Lab on a chip.

[89]  Micha E. Spira,et al.  Toward on-chip, in-cell recordings from cultured cardiomyocytes by arrays of gold mushroom-shaped microelectrodes , 2012, Front. Neuroeng..

[90]  C. Koch,et al.  The origin of extracellular fields and currents — EEG, ECoG, LFP and spikes , 2012, Nature Reviews Neuroscience.

[91]  D. Maclaurin,et al.  Optical recording of action potentials in mammalian neurons using a microbial rhodopsin , 2011, Nature Methods.

[92]  Aviad Hai,et al.  On-chip electroporation, membrane repair dynamics and transient in-cell recordings by arrays of gold mushroom-shaped microelectrodes. , 2012, Lab on a chip.