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Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts

Nature Nanotechnology volume 4, pages 126–133 (2009)Cite this article

Abstract

Carbon nanotubes have been applied in several areas of nerve tissue engineering to probe and augment cell behaviour, to label and track subcellular components, and to study the growth and organization of neural networks. Recent reports show that nanotubes can sustain and promote neuronal electrical activity in networks of cultured cells, but the ways in which they affect cellular function are still poorly understood. Here, we show, using single-cell electrophysiology techniques, electron microscopy analysis and theoretical modelling, that nanotubes improve the responsiveness of neurons by forming tight contacts with the cell membranes that might favour electrical shortcuts between the proximal and distal compartments of the neuron. We propose the ‘electrotonic hypothesis’ to explain the physical interactions between the cell and nanotube, and the mechanisms of how carbon nanotubes might affect the collective electrical activity of cultured neuronal networks. These considerations offer a perspective that would allow us to predict or engineer interactions between neurons and carbon nanotubes.

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Figure 1: The effect of nanotubes (CNTs) on neuronal excitability.
Figure 2: Planar electrically conductive surfaces do not affect after-potential neuronal excitability.
Figure 3: Effect of conductivity and nanoscale features on neurons.
Figure 4: The electrotonic hypothesis.
Figure 5: The ultrastructural interaction between multi-wall nanotubes and neurons.
Figure 6: Network-level correlate of ADP in single neurons: model and experiment.

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Acknowledgements

We are grateful to A. Roth, A. Schaefer and I. Riachi for helpful discussions, K.-H. Boven for providing ITO substrates, C. Zacchigna for assistance with tissue cultures, C. Gamboz and A. Mazzatenta for TEM procedures, and to L. Sivilotti for comments on the previous version of this manuscript. Financial support from EPFL (to M.G., L.G. and H.M.), EU (NEURONANO-NMP4-CT-2006-031847 to M.P., M.G., H.M. and L.B.), CARIPLO (to F.G.), Fondazione Alberto and Kathleen Casali, and Progetto D4 Area Science Park mobility program (to E.C.) is gratefully acknowledged.

Author information

Author notes

  1. Emanuele Cilia & Silvia Giordani

    Present address: Present address: Department of Biomedical Science, University of Antwerp, Universiteitsplein 1, B-2610 Wilrijk, Belgium (E.C.); School of Chemistry, Trinity College, Dublin College Green, Dublin 2, Ireland (S.G.),

  2. Michele Giugliano and Laura Ballerini: These authors contributed equally to this work

Authors and Affiliations

  1. Life Science Department, B.R.A.I.N., University of Trieste, via Fleming 22, Trieste, I-34127, Italy

    Giada Cellot, Emanuele Cilia, Vladimir Rancic, Antonella Sucapane & Laura Ballerini

  2. Department of Pharmaceutical Sciences, University of Trieste, Piazzale Europa 1, Trieste, I-34127, Italy

    Sara Cipollone, Silvia Giordani & Maurizio Prato

  3. Laboratory of Neural Microcircuitry, Brain Mind Institute, Ecole Polytechnique Fédérale de Lausanne, Station 15, Lausanne, CH-1015, Switzerland

    Luca Gambazzi, Henry Markram & Michele Giugliano

  4. Neurobiology Sector, International School for Advanced Studies (SISSA), via Beirut 2–4, Trieste, 34014, Italy

    Micaela Grandolfo

  5. ELETTRA Sincrotrone Trieste Strada Statale 14, Basovizza, Trieste, Italy

    Denis Scaini & Loredana Casalis

  6. Biosciences and Biotechnology Department, University of Milan-Bicocca, Piazza della Scienza 2, Milan, 20126, Italy

    Fabrizio Gelain

  7. Department of Biomedical Sciences, University of Antwerp, Universiteitsplein 1, Wilrijk, B-2610, Belgium

    Michele Giugliano

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Correspondence to Laura Ballerini.

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Cellot, G., Cilia, E., Cipollone, S. et al. Carbon nanotubes might improve neuronal performance by favouring electrical shortcuts. Nature Nanotech 4, 126–133 (2009). https://doi.org/10.1038/nnano.2008.374

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