Nanostructured gold microelectrodes for extracellular recording from electrogenic cells

We present a new biocompatible nanostructured microelectrode array for extracellular signal recording from electrogenic cells. Microfabrication techniques were combined with a template-assisted approach using nanoporous aluminum oxide to develop gold nanopillar electrodes. The nanopillars were approximately 300-400 nm high and had a diameter of 60 nm. Thus, they yielded a higher surface area of the electrodes resulting in a decreased impedance compared to planar electrodes. The interaction between the large-scale gold nanopillar arrays and cardiac muscle cells (HL-1) was investigated via focused ion beam milling. In the resulting cross-sections we observed a tight coupling between the HL-1 cells and the gold nanostructures. However, the cell membranes did not bend into the cleft between adjacent nanopillars due to the high pillar density. We performed extracellular potential recordings from HL-1 cells with the nanostructured microelectrode arrays. The maximal amplitudes recorded with the nanopillar electrodes were up to 100% higher than those recorded with planar gold electrodes. Increasing the aspect ratio of the gold nanopillars and changing the geometrical layout can further enhance the signal quality in the future.

[1]  U. Egert,et al.  A novel organotypic long-term culture of the rat hippocampus on substrate-integrated multielectrode arrays. , 1998, Brain research. Brain research protocols.

[2]  Michael L. Simpson,et al.  Tracking Gene Expression after DNA Delivery Using Spatially Indexed Nanofiber Arrays , 2004 .

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

[4]  M. Baudry,et al.  Advances in Network Electrophysiology , 2006 .

[5]  H. Masuda,et al.  Spatially Selective Metal Deposition into a Hole-Array Structure of Anodic Porous Alumina Using a Microelectrode , 1998 .

[6]  Ran Liu,et al.  Controlled electrochemical synthesis of conductive polymer nanotube structures. , 2007, Journal of the American Chemical Society.

[7]  Gang Li,et al.  Integration of Au Nanorods With Flexible Thin-Film Microelectrode Arrays for Improved Neural Interfaces , 2009 .

[8]  Jun Li,et al.  Vertically aligned carbon nanofiber arrays: an advance toward electrical-neural interfaces. , 2006, Small.

[9]  Shoso Shingubara,et al.  Fabrication of Nanomaterials Using Porous Alumina Templates , 2003 .

[10]  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.

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

[12]  Kornelius Nielsch,et al.  A template-based electrochemical method for the synthesis of multisegmented metallic nanotubes. , 2005, Angewandte Chemie.

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

[14]  N J Izzo,et al.  HL-1 cells: a cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Fan Yang,et al.  Robust cell migration and neuronal growth on pristine carbon nanotube sheets and yarns , 2007, Journal of biomaterials science. Polymer edition.

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

[17]  Andreas Offenhäusser,et al.  Extended Gate Electrode Arrays for Extracellular Signal Recordings , 2000 .

[18]  D. Mayer,et al.  Analyzing the electroactive surface of gold nanopillars by electrochemical methods for electrode miniaturization , 2008 .

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

[20]  Bruce C. Wheeler,et al.  Neural recording and stimulation of dissociated hippocampal cultures using microfabricated three-dimensional tip electrode array , 2006, Journal of Neuroscience Methods.

[21]  Nicholas A. Melosh,et al.  Gigaohm resistance membrane seals with stealth probe electrodes , 2010 .

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

[23]  M. Ericson,et al.  Vertically aligned carbon nanofiber arrays record electrophysiological signals from hippocampal slices. , 2007, Nano letters.

[24]  W. J. Stępniowski,et al.  Structural features of self-organized nanopore arrays formed by anodization of aluminum in oxalic acid at relatively high temperatures , 2009 .

[25]  T. Fisher,et al.  Lithography-free in situ Pd contacts to templated single-walled carbon nanotubes. , 2006, Nano letters.

[26]  Hongjie Dai,et al.  Neural stimulation with a carbon nanotube microelectrode array. , 2006, Nano letters.

[27]  Peidong Yang,et al.  Interfacing silicon nanowires with mammalian cells. , 2007, Journal of the American Chemical Society.

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

[29]  Kenji Fukuda,et al.  Ordered Metal Nanohole Arrays Made by a Two-Step Replication of Honeycomb Structures of Anodic Alumina , 1995, Science.

[30]  L. Berdondini,et al.  Cell-compatible array of three-dimensional tip electrodes for the detection of nitric oxide release. , 2005, Biosensors & bioelectronics.

[31]  M. Heuschkel,et al.  Power-law behavior of beat-rate variability in monolayer cultures of neonatal rat ventricular myocytes. , 2000, Circulation research.

[32]  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.

[33]  Ralf B. Wehrspohn,et al.  Self-ordering Regimes of Porous Alumina: The 10% Porosity Rule , 2002 .

[34]  C. Nguyen,et al.  Empirical study of unipolar and bipolar configurations using high resolution single multi-walled carbon nanotube electrodes for electrophysiological probing of electrically excitable cells , 2010, Nanotechnology.

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

[36]  Andreas Offenhäusser,et al.  Fabrication of large-scale patterned gold-nanopillar arrays on a silicon substrate using imprinted porous alumina templates. , 2006, Small.

[37]  Toshiaki Tamamura,et al.  Highly ordered nanochannel-array architecture in anodic alumina , 1997 .

[38]  M. Sander,et al.  Nanoparticle Arrays on Surfaces Fabricated Using Anodic Alumina Films as Templates , 2003 .

[39]  Yung-Chan Chen,et al.  Hydrophilic modification of neural microelectrode arrays based on multi-walled carbon nanotubes , 2010, Nanotechnology.

[40]  Yusuf Leblebici,et al.  Electrical modeling of the cell-electrode interface for recording neural activity from high-density microelectrode arrays , 2009, Neurocomputing.

[41]  Joseph J Pancrazio,et al.  Neural interfaces at the nanoscale. , 2008, Nanomedicine.

[42]  Jacob T. Robinson,et al.  Vertical silicon nanowires as a universal platform for delivering biomolecules into living cells , 2010, Proceedings of the National Academy of Sciences.

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

[44]  M. Dresselhaus,et al.  Nanowires and nanotubes , 2003 .

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

[46]  Mitchel J. Doktycz,et al.  Intracellular integration of synthetic nanostructures with viable cells for controlled biochemical manipulation , 2003 .

[47]  D. Bertrand,et al.  A three-dimensional multi-electrode array for multi-site stimulation and recording in acute brain slices , 2002, Journal of Neuroscience Methods.

[48]  C. R. Martin,et al.  Smart nanotubes for bioseparations and biocatalysis. , 2002, Journal of the American Chemical Society.