Abstract
Optogenetic silencing using light-driven ion fluxes permits rapid and effective inhibition of neural activity. Using rodent hippocampal neurons, we found that silencing activity with a chloride pump can increase the probability of synaptically evoked spiking after photoactivation; this did not occur with a proton pump. This effect can be accounted for by changes to the GABAA receptor reversal potential and demonstrates an important difference between silencing strategies.
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References
Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. Nat. Neurosci. 8, 1263–1268 (2005).
Zhang, F. et al. Nature 446, 633–639 (2007).
Zemelman, B.V., Lee, G.A., Ng, M. & Miesenböck, G. Neuron 33, 15–22 (2002).
Gradinaru, V. et al. J. Neurosci. 27, 14231–14238 (2007).
Fenno, L., Yizhar, O. & Deisseroth, K. Annu. Rev. Neurosci. 34, 389–412 (2011).
Tønnesen, J., Sørensen, A.T., Deisseroth, K., Lundberg, C. & Kokaia, M. Proc. Natl. Acad. Sci. USA 106, 12162–12167 (2009).
Gourine, A.V. et al. Science 329, 571–575 (2010).
Han, X. & Boyden, E.S. PLoS ONE 2, e299 (2007).
Chow, B.Y. et al. Nature 463, 98–102 (2010).
Mattis, J. et al. Nat. Methods 9, 159–172 (2012).
Gradinaru, V. et al. Cell 141, 154–165 (2010).
Madisen, L. et al. Nat. Neurosci. 15, 793–802 (2012).
Staley, K.J. & Proctor, W.R. J. Physiol. (Lond.) 519, 693–712 (1999).
Wright, R., Raimondo, J.V. & Akerman, C.J. Neural Plast. 2011, 728395 (2011).
Chesler, M. Physiol. Rev. 83, 1183–1221 (2003).
Stoppini, L., Buchs, P.A. & Muller, D. J. Neurosci. Methods 37, 173–182 (1991).
Tyzio, R., Holmes, G.L., Ben-Ari, Y. & Khazipov, R. Epilepsia 48, 96–105 (2007).
Streit, P., Thompson, S.M. & Gähwiler, B.H. Eur. J. Neurosci. 1, 603–615 (1989).
De Simoni, A., Griesinger, C.B. & Edwards, F.A. J. Physiol. (Lond.) 550, 135–147 (2003).
Olsen, S.R., Bortone, D.S., Adesnik, H. & Scanziani, M. Nature 483, 47–52 (2012).
Cardin, J.A. J. Physiol. Paris published online: doi:10.1016/j.jphysparis.2011.09.005 (19 September 2011).
Hartmann, A.M. & Nothwang, H.G. BMC Res. Notes 4, 526 (2011).
Pouille, F. & Scanziani, M. Science 293, 1159–1163 (2001).
Ascoli, G.A., Gasparini, S., Medinilla, V. & Migliore, M. J. Neurosci. 30, 6434–6442 (2010).
Jin, X., Huguenard, J.R. & Prince, D.A. J. Neurophysiol. 93, 2117–2126 (2005).
Acknowledgements
We thank P. Bolam (Oxford University) for resources, and K. Deisseroth (Stanford University) and E. Boyden (Massachusetts Institute of Technology) for DNA constructs. We also thank G. Miesenböck, D. Kätzel and B. Richards for comments. Supported by a grant from the Medical Research Council (G0601503); research leading to these results received funding under the European Community's Seventh Framework Programme (FP7/2007-2013).
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J.V.R. and C.J.A. designed the research. J.V.R., T.J.E. and L.K. performed the experiments. J.V.R. and C.J.A. analyzed the data. J.V.R. and C.J.A. wrote the paper.
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Raimondo, J., Kay, L., Ellender, T. et al. Optogenetic silencing strategies differ in their effects on inhibitory synaptic transmission. Nat Neurosci 15, 1102–1104 (2012). https://doi.org/10.1038/nn.3143
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DOI: https://doi.org/10.1038/nn.3143
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