Nanoelectronics for Neuroscience

Characterizing the electrical activity between neuronal cells is crucial in understanding the complex processes in the brain, both in healthy and diseased tissue. Neural interface technology that enables recording of the neuronal electrical activity as well as stimulation of the neurons has attracted great attention for both experimental and clinical applications. In this article, we discuss the fundamentals of the bioelectrical signals recording, and the advancements in the field of nano-bioelectronics, that is, the different kinds of materials and designs used to improve the cellular-device interface to enable recording and stimulation of the neuronal cells. Furthermore, we discuss the development of synthetic biomaterials that enable fusion of electronics and bioactive scaffolds which are essential to regenerative engineering. We also discuss the technical and scientific challenges associated with these technologies, and the future prospects and opportunities.

[1]  P. Fromherz,et al.  Signal transmission from individual mammalian nerve cell to field-effect transistor. , 2005, Small.

[2]  Charles M Lieber,et al.  Graphene and nanowire transistors for cellular interfaces and electrical recording. , 2010, Nano letters.

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

[4]  Alberto Diaspro,et al.  Brain Function: Novel Technologies Driving Novel Understanding , 2014 .

[5]  A. Hodgkin,et al.  The effect of sodium ions on the electrical activity of the giant axon of the squid , 1949, The Journal of physiology.

[6]  Peter Fromherz,et al.  Transistor array with an organotypic brain slice: field potential records and synaptic currents , 2002, The European journal of neuroscience.

[7]  E. Chichilnisky,et al.  Large-area microelectrode arrays for recording of neural signals , 2004, IEEE Transactions on Nuclear Science.

[8]  F. Toma,et al.  Multiwalled carbon-nanotube-functionalized microelectrode arrays fabricated by microcontact printing: platform for studying chemical and electrical neuronal signaling. , 2011, Small.

[9]  A. Hodgkin,et al.  The dual effect of membrane potential on sodium conductance in the giant axon of Loligo , 1952, The Journal of physiology.

[10]  Bruce C. Wheeler,et al.  Microelectrode Array Recordings of Patterned Hippocampal Neurons for Four Weeks , 2000 .

[11]  SUPARNA DUTTASINHA,et al.  Graphene: Status and Prospects , 2009, Science.

[12]  G. Pfurtscheller,et al.  Brain-Computer Interfaces for Communication and Control. , 2011, Communications of the ACM.

[13]  K. Wise,et al.  Performance of planar multisite microprobes in recording extracellular single-unit intracortical activity , 1988, IEEE Transactions on Biomedical Engineering.

[14]  D. Edell,et al.  Factors influencing the biocompatibility of insertable silicon microshafts in cerebral cortex , 1992, IEEE Transactions on Biomedical Engineering.

[15]  F. Bezanilla.  The action potential: from voltage-gated conductances to molecular structures. , 2006, Biological research.

[16]  A. Lambacher,et al.  Electrical imaging of neuronal activity by multi-transistor-array (MTA) recording at 7.8 μm resolution , 2004 .

[17]  Jonathan R Wolpaw,et al.  Control of a two-dimensional movement signal by a noninvasive brain-computer interface in humans. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[18]  F. A. Edwards,et al.  A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system , 1989, Pflügers Archiv.

[19]  P. Fromherz.  Electrical interfacing of nerve cells and semiconductor chips. , 2002, Chemphyschem : a European journal of chemical physics and physical chemistry.

[20]  Patrick A Tresco,et al.  The brain tissue response to implanted silicon microelectrode arrays is increased when the device is tethered to the skull. , 2007, Journal of biomedical materials research. Part A.

[21]  Justin A. Blanco,et al.  Dissolvable films of silk fibroin for ultrathin conformal bio-integrated electronics. , 2010, Nature materials.

[22]  David C. Martin,et al.  Chronic neural recordings using silicon microelectrode arrays electrochemically deposited with a poly(3,4-ethylenedioxythiophene) (PEDOT) film , 2006, Journal of neural engineering.

[23]  Ann Marie Craig,et al.  NMDA Receptor Subunits Have Differential Roles in Mediating Excitotoxic Neuronal Death Both In Vitro and In Vivo , 2007, The Journal of Neuroscience.

[24]  D. Szarowski,et al.  Cerebral Astrocyte Response to Micromachined Silicon Implants , 1999, Experimental Neurology.

[25]  M. Spira,et al.  Multi-electrode array technologies for neuroscience and cardiology. , 2013, Nature nanotechnology.

[26]  A. Offenhäusser,et al.  Cell-transistor hybrid systems and their potential applications. , 2001, Trends in biotechnology.

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

[28]  E. Marg,et al.  Indwelling multiple micro-electrodes in the brain. , 1967, Electroencephalography and clinical neurophysiology.

[29]  Sigurd Wagner,et al.  Characterization of an Elastically Stretchable Microelectrode Array and Its Application to Neural Field Potential Recordings , 2009 .

[30]  Jerald D. Kralik,et al.  Techniques for long-term multisite neuronal ensemble recordings in behaving animals. , 2001, Methods.

[31]  R. Llinás.  The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[32]  Andre K. Geim,et al.  Electric Field Effect in Atomically Thin Carbon Films , 2004, Science.

[33]  Luca Berdondini,et al.  Emergent Functional Properties of Neuronal Networks with Controlled Topology , 2012, PloS one.

[34]  Tian-Ming Fu,et al.  Nanoelectronics-biology frontier: From nanoscopic probes for action potential recording in live cells to three-dimensional cyborg tissues. , 2013, Nano today.

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

[36]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.

[37]  Dong-il Dan Cho,et al.  Roughened polysilicon for low impedance microelectrodes in neural probes , 2003 .

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

[39]  S. Cogan.  Neural stimulation and recording electrodes. , 2008, Annual review of biomedical engineering.

[40]  A. Hodgkin,et al.  Propagation of electrical signals along giant nerve fibres , 1952, Proceedings of the Royal Society of London. Series B - Biological Sciences.

[41]  B. Wheeler,et al.  Recording from the Aplysia Abdominal Ganglion with a Planar Microelectrode Array , 1986, IEEE Transactions on Biomedical Engineering.

[42]  T G Yuen,et al.  Histological evaluation of polyesterimide-insulated gold wires in brain. , 1995, Biomaterials.

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

[44]  Diego Contreras,et al.  Electrophysiological classes of neocortical neurons , 2004, Neural Networks.

[45]  F. Solzbacher,et al.  Integrated wireless neural interface based on the Utah electrode array , 2009, Biomedical microdevices.

[46]  P. Fromherz,et al.  Silicon Chip Interfaced with a Geometrically Defined Net of Snail Neurons , 2005 .

[47]  Shashi K. Murthy,et al.  Bridging the Divide between Neuroprosthetic Design, Tissue Engineering and Neurobiology , 2009, Front. Neuroeng..

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

[49]  Henry Markram,et al.  Substrate Arrays of Iridium Oxide Microelectrodes for in Vitro Neuronal Interfacing , 2008, Front. Neuroeng..

[50]  Stefano Vassanelli,et al.  Transistor Probes Local Potassium Conductances in the Adhesion Region of Cultured Rat Hippocampal Neurons , 1999, The Journal of Neuroscience.

[51]  M. Häusser,et al.  Electrophysiology in the age of light , 2009, Nature.

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

[53]  Eshel Ben-Jacob,et al.  Electro-chemical and biological properties of carbon nanotube based multi-electrode arrays , 2007, Nanotechnology.

[54]  Benjamin F. Grewe,et al.  Cellular Level Brain Imaging in Behaving Mammals: An Engineering Approach , 2015, Neuron.

[55]  David C. Martin,et al.  Neuronal cell loss accompanies the brain tissue response to chronically implanted silicon microelectrode arrays , 2005, Experimental Neurology.

[56]  Xuan Cheng,et al.  Poly(3,4-ethylenedioxythiophene)/multiwall carbon nanotube composite coatings for improving the stability of microelectrodes in neural prostheses applications. , 2013, Acta biomaterialia.

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

[58]  Ikuro Suzuki,et al.  Carbon nanotube multi-electrode array chips for noninvasive real-time measurement of dopamine, action potentials, and postsynaptic potentials. , 2013, Biosensors & bioelectronics.

[59]  M. Farah,et al.  Progress and challenges in probing the human brain , 2015, Nature.

[60]  D. Robinson,et al.  The electrical properties of metal microelectrodes , 1968 .

[61]  Yoonkey Nam,et al.  Gold nanograin microelectrodes for neuroelectronic interfaces. , 2013, Biotechnology journal.

[62]  Andreas Offenhäusser,et al.  Neuron–transistor coupling: interpretation of individual extracellular recorded signals , 2005, European Biophysics Journal.

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

[64]  Jerald D. Kralik,et al.  Chronic, multisite, multielectrode recordings in macaque monkeys , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[65]  E. Evarts.  Pyramidal tract activity associated with a conditioned hand movement in the monkey. , 1966, Journal of neurophysiology.

[66]  K D Wise,et al.  Microfabrication techniques for integrated sensors and microsystems. , 1991, Science.

[67]  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.

[68]  Piet Bergveld,et al.  Extracellular Potential Recordings by Means of a Field Effect Transistor Without Gate Metal, Called OSFET , 1976, IEEE Transactions on Biomedical Engineering.

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

[70]  Areles Molleman,et al.  Patch Clamping: An Introductory Guide To Patch Clamp Electrophysiology , 2002 .

[71]  Amir M. Sodagar,et al.  Microelectrodes, Microelectronics, and Implantable Neural Microsystems , 2008, Proceedings of the IEEE.

[72]  M. Abidian,et al.  A Review of Organic and Inorganic Biomaterials for Neural Interfaces , 2014, Advanced materials.

[73]  J M Carmena,et al.  In Vitro and In Vivo Evaluation of PEDOT Microelectrodes for Neural Stimulation and Recording , 2011, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

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

[75]  Charles M. Lieber,et al.  Macroporous nanowire nanoelectronic scaffolds for synthetic tissues. , 2012, Nature materials.

[76]  J. Rothwell.  Principles of Neural Science , 1982 .

[77]  Stefano Vassanelli,et al.  Transistor records of excitable neurons from rat brain , 1998 .

[78]  R. Normann,et al.  Chronic recording capability of the Utah Intracortical Electrode Array in cat sensory cortex , 1998, Journal of Neuroscience Methods.

[79]  Charles M. Lieber,et al.  Semiconductor nanowires: A platform for nanoscience and nanotechnology , 2010, 2010 3rd International Nanoelectronics Conference (INEC).

[80]  Robert H. Lee,et al.  Three-dimensional neural constructs: a novel platform for neurophysiological investigation , 2008, Journal of neural engineering.

[81]  Thomas M. McKenna,et al.  Enabling Technologies for Cultured Neural Networks , 1994 .

[82]  Jared P. Ness,et al.  Graphene-based carbon-layered electrode array technology for neural imaging and optogenetic applications , 2014, Nature Communications.

[83]  Michael D Joseph,et al.  Poly(3,4-ethylenedioxythiophene) (PEDOT) polymer coatings facilitate smaller neural recording electrodes , 2011, Journal of neural engineering.

[84]  N.F. de Rooij,et al.  Microelectrode arrays for electrophysiological monitoring of hippocampal organotypic slice cultures , 1997, IEEE Transactions on Biomedical Engineering.

[85]  A. Offenhäusser,et al.  Field-effect transistor array for monitoring electrical activity from mammalian neurons in culture. , 1997, Biosensors & bioelectronics.

[86]  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.

[87]  T. Lucas,et al.  Transparent and flexible low noise graphene electrodes for simultaneous electrophysiology and neuroimaging , 2014, Nature Communications.

[88]  J. Nicholls.  From neuron to brain , 1976 .

[89]  H. Curtis,et al.  ELECTRIC IMPEDANCE OF THE SQUID GIANT AXON DURING ACTIVITY , 1939, The Journal of general physiology.

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

[91]  A. Hodgkin,et al.  Currents carried by sodium and potassium ions through the membrane of the giant axon of Loligo , 1952, The Journal of physiology.

[92]  L. Paninski,et al.  Information about movement direction obtained from synchronous activity of motor cortical neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Gustaaf Borghs,et al.  Electrochemical deposition of polypyrrole/graphene oxide composite on microelectrodes towards tuning the electrochemical properties of neural probes , 2011 .

[94]  David C. Martin,et al.  Fuzzy gold electrodes for lowering impedance and improving adhesion with electrodeposited conducting polymer films , 2003 .

[95]  Gengfeng Zheng,et al.  Detection, Stimulation, and Inhibition of Neuronal Signals with High-Density Nanowire Transistor Arrays , 2006, Science.

[96]  P. Tresco,et al.  Response of brain tissue to chronically implanted neural electrodes , 2005, Journal of Neuroscience Methods.

[97]  Zhigang Suo,et al.  Syringe-injectable electronics. , 2015, Nature nanotechnology.

[98]  A. Hodgkin,et al.  The components of membrane conductance in the giant axon of Loligo , 1952, The Journal of physiology.

[99]  Gilles Clermont,et al.  THE ROLE OF INITIAL TRAUMA IN THE HOST'S RESPONSE TO INJURY AND HEMORRHAGE: INSIGHTS FROM A CORRELATION OF MATHEMATICAL SIMULATIONS AND HEPATIC TRANSCRIPTOMIC ANALYSIS , 2006, Shock.

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

[101]  P Bergveld,et al.  Development of an ion-sensitive solid-state device for neurophysiological measurements. , 1970, IEEE transactions on bio-medical engineering.

[102]  A. Hodgkin,et al.  Resting and action potentials in single nerve fibres , 1945, The Journal of physiology.

[103]  A. Hodgkin,et al.  Measurement of current‐voltage relations in the membrane of the giant axon of Loligo , 1952, The Journal of physiology.

[104]  P. Fromherz,et al.  A neuron-silicon junction: a Retzius cell of the leech on an insulated-gate field-effect transistor. , 1991, Science.

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

[106]  R. D. Purves,et al.  Microelectrode methods for intracellular recording and ionophoresis , 1981 .

[107]  S. Sombati,et al.  Effects of Topiramate on Sustained Repetitive Firing and Spontaneous Recurrent Seizure Discharges in Cultured Hippocampal Neurons , 2000, Epilepsia.

[108]  Y. Tai,et al.  The neurochip: a new multielectrode device for stimulating and recording from cultured neurons , 1999, Journal of Neuroscience Methods.

[109]  Weis,et al.  Neuron adhesion on a silicon chip probed by an array of field-effect transistors. , 1996, Physical review letters.

[110]  Sergio Martinoia,et al.  Functional connectivity and dynamics of cortical–thalamic networks co-cultured in a dual compartment device , 2012, Journal of neural engineering.

[111]  Charles M. Lieber,et al.  Synthetic nanoelectronic probes for biological cells and tissues. , 2013, Annual review of analytical chemistry.

[112]  J. Hetke,et al.  Surface modification of neural recording electrodes with conducting polymer/biomolecule blends. , 2001, Journal of biomedical materials research.

[113]  Daryl R Kipke,et al.  Advanced Neurotechnologies for Chronic Neural Interfaces: New Horizons and Clinical Opportunities , 2008, The Journal of Neuroscience.

[114]  Simon R. Cherry,et al.  In vivo imaging of neuronal activation and plasticity in the rat brain by high resolution positron emission tomography (microPET) , 2000, Nature Biotechnology.

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

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

[117]  J. Donoghue,et al.  Neuronal Interactions Improve Cortical Population Coding of Movement Direction , 1999, The Journal of Neuroscience.

[118]  Miguel A. L. Nicolelis,et al.  Brain–machine interfaces: past, present and future , 2006, Trends in Neurosciences.

[119]  D. Szarowski,et al.  Brain responses to micro-machined silicon devices , 2003, Brain Research.

[120]  Samouil L. Farhi,et al.  All-optical electrophysiology in mammalian neurons using engineered microbial rhodopsins , 2014, Nature Methods.

[121]  Vincent Torre,et al.  Toward the neurocomputer: image Processing and pattern recognition with neuronal cultures , 2005, IEEE Transactions on Biomedical Engineering.