Using Ca2+ imaging in freely behaving mice that repeatedly explored a familiar environment, we tracked thousands of CA1 pyramidal cells' place fields over weeks. Place coding was dynamic, as each day the ensemble representation of this environment involved a unique subset of cells. However, cells in the ∼15–25% overlap between any two of these subsets retained the same place fields, which sufficed to preserve an accurate spatial representation across weeks.
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O'Keefe, J.N.L. The Hippocampus as a Cognitive Map (Clarendon, 1978).
Leutgeb, S. et al. Science 309, 619–623 (2005).
Muller, R.U., Kubie, J.L. & Ranck, J.B. Jr. J. Neurosci. 7, 1935–1950 (1987).
Thompson, L.T. & Best, P.J. Brain. Res. 509, 299–308 (1990).
Kentros, C. et al. Science 280, 2121–2126 (1998).
Lever, C., Wills, T., Cacucci, F., Burgess, N. & O'Keefe, J. Nature 416, 90–94 (2002).
Kentros, C.G., Agnihotri, N.T., Streater, S., Hawkins, R.D. & Kandel, E.R. Neuron 42, 283–295 (2004).
Cacucci, F., Wills, T.J., Lever, C., Giese, K.P. & O'Keefe, J. J. Neurosci. 27, 7854–7859 (2007).
Muzzio, I.A. et al. PLoS Biol. 7, e1000140 (2009).
Tian, L. et al. Nat. Methods 6, 875–881 (2009).
Barretto, R.P. et al. Nat. Med. 17, 223–228 (2011).
Ghosh, K.K. et al. Nat. Methods 8, 871–878 (2011).
Mukamel, E.A., Nimmerjahn, A. & Schnitzer, M.J. Neuron 63, 747–760 (2009).
Dombeck, D.A., Harvey, C.D., Tian, L., Looger, L.L. & Tank, D.W. Nat. Neurosci. 13, 1433–1440 (2010).
McHugh, T.J., Blum, K.I., Tsien, J.Z., Tonegawa, S. & Wilson, M.A. Cell 87, 1339–1349 (1996).
Markus, E.J., Barnes, C.A., McNaughton, B.L., Gladden, V.L. & Skaggs, W.E. Hippocampus 4, 410–421 (1994).
Nakazawa, K. et al. Neuron 38, 305–315 (2003).
Rotenberg, A., Mayford, M., Hawkins, R.D., Kandel, E.R. & Muller, R.U. Cell 87, 1351–1361 (1996).
Lisman, J.E. Trends Neurosci. 20, 38–43 (1997).
Gradinaru, V. et al. J. Neurosci. 27, 14231–14238 (2007).
Barretto, R.P., Messerschmidt, B. & Schnitzer, M.J. Nat. Methods 6, 511–512 (2009).
Barretto, R.P.J. & Schnitzer, M.J. in Imaging: a Laboratory Manual (ed. R. Yuste) Ch. 50 (Cold Spring Harbor Laboratory Press, 2011).
Thévenaz, P., Ruttimann, U.E. & Unser, M. IEEE Trans. Image Process. 7, 27–41 (1998).
Nimmerjahn, A., Mukamel, E.A. & Schnitzer, M.J. Neuron 62, 400–412 (2009).
Shannon, C.E. & Weaver, W. The Mathematical Theory of Communication (University of Illinois Press, 1949).
Brown, E.N., Frank, L.M., Tang, D., Quirk, M.C. & Wilson, M.A. J. Neurosci. 18, 7411–7425 (1998).
Quian Quiroga, R. & Panzeri, S. Nat. Rev. Neurosci. 10, 173–185 (2009).
We thank L. Looger (Janelia Farm Research Campus) for GCaMP3 plasmid, and A. Attardo, T. Davidson, J. Fitzgerald, J. Li, J.Z. Li, A. Lui, C. Ramachandran, O. Yizhar and T. Zhang for conversations and assistance. We appreciate fellowships from the US National Science Foundation (L.D.B., L.J.K.), the Simons (L.J.K.) and Machiah (Y.Z.) Foundations and research funding to M.J.S. from the Paul G. Allen Family Foundation and the US National Institutes of Health (grants DP1OD003560, R21AG038771 and R21MH099469).
E.D.C., K.K.G. and L.D.B. are now full-time employees of Inscopix Inc., a company that has exclusive license to and is commercializing the integrated microscope technology. Y.Z., L.D.B., E.D.C., K.K.G., A.E.G. and M.J.S. have equity interests in Inscopix. Y.Z., A.E.G. and M.J.S. are consultants to Inscopix.
Supplementary Figures 1–8 (PDF 2196 kb)
Ca2+-imaging in hundreds of CA1 pyramidal cells in a freely behaving mouse. A video showing a mouse exploring a circular arena (left panel) and the simultaneously acquired brain-imaging data of CA1 pyramidal cell Ca2+ activity, displayed as relative changes in fluorescence (ΔF/F) (right panel). 705 pyramidal cells were identified in the total data set and correspond to the neurons of Fig. 1b. The Ca2+-imaging frame rate was 20 Hz, but these data are shown down-sampled to 5 Hz to aid visualization of the Ca2+ transients. The video playback rate is sped up four-fold from how the events actually occurred. (MOV 22073 kb)
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Ziv, Y., Burns, L., Cocker, E. et al. Long-term dynamics of CA1 hippocampal place codes. Nat Neurosci 16, 264–266 (2013). https://doi.org/10.1038/nn.3329
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