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Recording spikes from a large fraction of the ganglion cells in a retinal patch

Abstract

To understand a neural circuit completely requires simultaneous recording from most of the neurons in that circuit. Here we report recording and spike sorting techniques that enable us to record from all or nearly all of the ganglion cells in a patch of the retina. With a dense multi-electrode array, each ganglion cell produces a unique pattern of activity on many electrodes when it fires an action potential. Signals from all of the electrodes are combined with an iterative spike sorting algorithm to resolve ambiguities arising from overlapping spike waveforms. We verify that we are recording from a large fraction of ganglion cells over the array by labeling the ganglion cells with a retrogradely transported dye and by comparing the number of labeled and recorded cells. Using these methods, we show that about 60 receptive fields of ganglion cells cover each point in visual space in the salamander, consistent with anatomical findings.

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Figure 1: The dense array.
Figure 2: Identifying spike templates.
Figure 3: Matching templates to the raw data.
Figure 4: Evaluating the method.
Figure 5: Axonal versus somatic spikes.
Figure 6: Effects of splitting one cell into two templates.
Figure 7: Example of two nearby ganglion cells.
Figure 8: Receptive field sizes of ganglion cells.

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References

  1. Rodieck, R.W. The First Steps in Seeing (Sinauer Associates, Sunderland, Massachusetts, USA, 1998).

    Google Scholar 

  2. Meister, M., Pine, J. & Baylor, D.A. Multi-neuronal signals from the retina: acquisition and analysis. J. Neurosci. Methods 51, 95–106 (1994).

    Article  CAS  Google Scholar 

  3. Schnitzer, M.J. & Meister, M. Multineuronal firing patterns in the signal from eye to brain. Neuron 37, 499–511 (2003).

    Article  CAS  Google Scholar 

  4. DeVries, S.H. & Baylor, D.A. Mosaic arrangement of ganglion cell receptive fields in rabbit retina. J. Neurophysiol. 78, 2048–2060 (1997).

    Article  CAS  Google Scholar 

  5. Lewicki, M.S. A review of methods for spike sorting: the detection and classification of neural action potentials. Network 9, R53–R78 (1998).

    Article  CAS  Google Scholar 

  6. Hulata, E., Segev, R. & Ben-Jacob, E. A method for spike sorting and detection based on wavelet packets and Shannon's mutual information. J. Neurosci. Methods 117, 1–12 (2002).

    Article  PubMed  Google Scholar 

  7. Atiya, A.F. Recognition of multiunit neural signals. IEEE Trans. Biomed. Eng. 39, 723–729 (1992).

    Article  CAS  Google Scholar 

  8. Gray, C.M., Maldonado, P.E., Wilson, M. & McNaughton, B. Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J. Neurosci. Methods 63, 43–54 (1995).

    Article  CAS  Google Scholar 

  9. Fee, M.S., Mitra, P.P. & Kleinfeld, D. Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-gaussian variability. J. Neurosci. Methods 69, 175–188 (1996).

    Article  CAS  Google Scholar 

  10. Henze, D.A. et al. Intracellular features predicted by extracellular recordings in the hippocampus in vivo. J. Neurophysiol. 84, 390–400 (2000).

    Article  CAS  Google Scholar 

  11. Watt, C.B., Yang, S.Z., Lam, D.M. & Wu, S.M. Localization of tyrosine-hydroxylase-like-immunoreactive amacrine cells in the larval tiger salamander retina. J. Comp. Neurol. 272, 114–126 (1988).

    Article  CAS  Google Scholar 

  12. Zhang, J. & Wu, S.M. Immunocytochemical analysis of cholinergic amacrine cells in the tiger salamander retina. NeuroReport 12, 1371–1375 (2001).

    Article  CAS  Google Scholar 

  13. Zhang, J., Yang, Z. & Wu, S.M. Immunocytochemical analysis of spatial organization of photoreceptors and amacrine and ganglion cells in the tiger salamander retina. Vis. Neurosci. 21, 157–166 (2004).

    Article  Google Scholar 

  14. Sakai, H.M., Machuca, H. & Naka, K.I. Processing of color- and noncolor-coded signals in the gourami retina. II. Amacrine cells. J. Neurophysiol. 78, 2018–2033 (1997).

    Article  CAS  Google Scholar 

  15. Cleland, B.G. & Levick, W.R. Brisk and sluggish concentrically organized ganglion cells in the cat's retina. J. Physiol. (Lond.) 240, 421–456 (1974).

    Article  CAS  Google Scholar 

  16. Cleland, B.G. & Levick, W.R. Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. J. Physiol. (Lond.) 240, 457–492 (1974).

    Article  CAS  PubMed  Google Scholar 

  17. Toris, C.B., Eiesland, J.L. & Miller, R.F. Morphology of ganglion cells in the neotenous tiger salamander retina. J. Comp. Neurol. 352, 535–559 (1995).

    Article  CAS  Google Scholar 

  18. Sun, W., Li, N. & He, S. Large-scale morphological survey of mouse retinal ganglion cells. J. Comp. Neurol. 451, 115–126 (2002).

    Article  Google Scholar 

  19. Rockhill, R.L., Daly, F.J., MacNeil, M.A., Brown, S.P. & Masland, R.H. The diversity of ganglion cells in a mammalian retina. J. Neurosci. 22, 3831–3843 (2002).

    Article  CAS  Google Scholar 

  20. Wässle, H. & Boycott, B.B. Functional architecture of the mammalian retina. Physiol. Rev. 71, 447–480 (1991).

    Article  Google Scholar 

  21. Lewicki, M.S. Bayesian modeling and classification of neural signals. Neural Comput. 6, 1005–1030 (1994).

    Article  Google Scholar 

  22. Hulata, E., Segev, R., Shapira, Y., Benveniste, M. & Ben-Jacob, E. Detection and sorting of neural spikes using wavelet packets. Phys. Rev. Lett. 85, 4637–4640 (2000).

    Article  CAS  Google Scholar 

  23. Wheeler, B.C. & Smith, S.R. High-resolution alignment of action potential waveforms using cubic spline interpolation. J. Biomed. Eng. 10, 47–53 (1988).

    Article  CAS  Google Scholar 

  24. Yang, X.W. & Shamma, S.A. A totally automated system for the detection and classification of neural spikes. IEEE Trans. Biomed. Eng. 35, 806–816 (1988).

    Article  CAS  Google Scholar 

  25. Wheeler, B.C. & Brewer, G.J. Multineuron patterning and recording. Enabling Technologies for Culturing Neural Networks (eds. Stenger, D.A. & McKenna, T.M.) 167–185 (Academic, San Diego, California, USA, 1994).

    Google Scholar 

  26. McNaughton, B.L., O'Keefe, J. & Barnes, C.A. The stereotrode: a new technique for simultaneous isolation of several single units in the central nervous system from multiple unit records. J. Neurosci. Methods 8, 391–397 (1983).

    Article  CAS  Google Scholar 

  27. Vetter, R.J., Williams, J.C., Hetke, J.F., Nunamaker, E.A. & Kipke, D.R. Chronic neural recording using silicon-substrate microelectrode arrays implanted in cerebral cortex. IEEE Trans. Biomed. Eng. 51, 896–904 (2004).

    Article  Google Scholar 

  28. Balasubramanian, V. & Berry, M.J. A test of metabolically efficient coding in the retina. Network 13, 531–552 (2002).

    Article  Google Scholar 

  29. Dacey, D.M., Peterson, B.B., Robinson, F.R. & Gamlin, P.D. Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37, 15–27 (2003).

    Article  CAS  Google Scholar 

  30. Roth, G. Visual Behavior in Salamanders (Springer, Berlin, 1987).

    Book  Google Scholar 

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Acknowledgements

We thank P. Sterling, D. Tank, A. Fairhall and S. Shoham for discussion; P. Bisher for help with confocal imaging and electron microscopy; and R. Harris and G. Lewen for assistance with data acquisition. This work was supported by a grant from the National Eye Institute (R01 EY14196) and a Pew Scholars Award to M.J.B.

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Correspondence to Michael J Berry II.

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Segev, R., Goodhouse, J., Puchalla, J. et al. Recording spikes from a large fraction of the ganglion cells in a retinal patch. Nat Neurosci 7, 1155–1162 (2004). https://doi.org/10.1038/nn1323

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