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Origin of correlated activity between parasol retinal ganglion cells

Nature Neuroscience volume 11, pages 1343–1351 (2008)Cite this article

Abstract

Cells throughout the CNS have synchronous activity patterns; that is, a cell's probability of generating an action potential depends both on its firing rate and on the occurrence of action potentials in surrounding cells. The mechanisms producing synchronous or correlated activity are poorly understood despite its prevalence and potential effect on neural coding. We found that neighboring parasol ganglion cells in primate retina received strongly correlated synaptic input in the absence of modulated light stimuli. This correlated variability appeared to arise through the same circuits that provide uncorrelated synaptic input. In addition, ON, but not OFF, parasol cells were coupled electrically. Correlated variability in synaptic input, however, dominated correlations in the parasol spike outputs and shared variability in the timing of action potentials generated by neighboring cells. These results provide a mechanistic picture of how correlated activity is produced in a population of neurons that are critical for visual perception.

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Figure 1: Correlated variability in the synaptic inputs to neighboring ON and OFF parasol cells.
Figure 2: OFF parasol cells receive less tonic excitatory input than ON parasol cells.
Figure 3: Common noise in the excitatory synaptic inputs to OFF, but not ON, parasol cells depends on stimulus properties.
Figure 4: Correlations in the inhibitory synaptic inputs to ON and OFF parasol cells.
Figure 5: ON, but not OFF, cells are effectively reciprocally coupled.
Figure 6: Contributions of common noise and reciprocal connections to correlations between spike trains of ON parasol cells.
Figure 7: Correlations affect temporal precision of ganglion cell spike responses.

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References

  1. Usrey, W.M. & Reid, R.C. Synchronous activity in the visual system. Annu. Rev. Physiol. 61, 435–456 (1999).

    Article  CAS  Google Scholar 

  2. Averbeck, B.B., Latham, P.E. & Pouget, A. Neural correlations, population coding and computation. Nat. Rev. Neurosci. 7, 358–366 (2006).

    Article  CAS  Google Scholar 

  3. Meister, M., Lagnado, L. & Baylor, D.A. Concerted signaling by retinal ganglion cells. Science 270, 1207–1210 (1995).

    Article  CAS  Google Scholar 

  4. Dan, Y., Alonso, J.M., Usrey, W.M. & Reid, R.C. Coding of visual information by precisely correlated spikes in the lateral geniculate nucleus. Nat. Neurosci. 1, 501–507 (1998).

    Article  CAS  Google Scholar 

  5. Pillow, J.W. et al. Spatio-temporal correlations and visual signaling in a complete neuronal population. Nature 454, 995–999 (2008).

    Article  CAS  Google Scholar 

  6. Romo, R., Hernandez, A., Zainos, A. & Salinas, E. Correlated neuronal discharges that increase coding efficiency during perceptual discrimination. Neuron 38, 649–657 (2003).

    Article  CAS  Google Scholar 

  7. Zohary, E., Shadlen, M.N. & Newsome, W.T. Correlated neuronal discharge rate and its implications for psychophysical performance. Nature 370, 140–143 (1994).

    Article  CAS  Google Scholar 

  8. Petersen, R.S., Panzeri, S. & Diamond, M.E. Population coding of stimulus location in rat somatosensory cortex. Neuron 32, 503–514 (2001).

    Article  CAS  Google Scholar 

  9. Puchalla, J.L., Schneidman, E., Harris, R.A. & Berry, M.J. Redundancy in the population code of the retina. Neuron 46, 493–504 (2005).

    Article  CAS  Google Scholar 

  10. Nirenberg, S., Carcieri, S.M., Jacobs, A.L. & Latham, P.E. Retinal ganglion cells act largely as independent encoders. Nature 411, 698–701 (2001).

    Article  CAS  Google Scholar 

  11. Mastronarde, D.N. Correlated firing of retinal ganglion cells. Trends Neurosci. 12, 75–80 (1989).

    Article  CAS  Google Scholar 

  12. Meister, M. Multineuronal codes in retinal signaling. Proc. Natl. Acad. Sci. USA 93, 609–614 (1996).

    Article  CAS  Google Scholar 

  13. Field, G.D. & Chichilnisky, E.J. Information processing in the primate retina: circuitry and coding. Annu. Rev. Neurosci. 30, 1–30 (2007).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  15. Schneidman, E., Berry, M.J. 2nd., Segev, R. & Bialek, W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440, 1007–1012 (2006).

    Article  CAS  Google Scholar 

  16. Shlens, J. et al. The structure of multi-neuron firing patterns in primate retina. J. Neurosci. 26, 8254–8266 (2006).

    Article  CAS  Google Scholar 

  17. Vaney, D.I. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci. Lett. 125, 187–190 (1991).

    Article  CAS  Google Scholar 

  18. Dacey, D.M. & Brace, S. A coupled network for parasol, but not midget, ganglion cells in the primate retina. Vis. Neurosci. 9, 279–290 (1992).

    Article  CAS  Google Scholar 

  19. Mastronarde, D.N. Correlated firing of cat retinal ganglion cells. I. Spontaneously active inputs to X- and Y-cells. J. Neurophysiol. 49, 303–324 (1983).

    Article  CAS  Google Scholar 

  20. Mastronarde, D.N. Correlated firing of cat retinal ganglion cells. II. Responses of X- and Y-cells to single quantal events. J. Neurophysiol. 49, 325–349 (1983).

    Article  CAS  Google Scholar 

  21. Mastronarde, D.N. Interactions between ganglion cells in cat retina. J. Neurophysiol. 49, 350–365 (1983).

    Article  CAS  Google Scholar 

  22. Jacoby, R., Stafford, D., Kouyama, N. & Marshak, D. Synaptic inputs to ON parasol ganglion cells in the primate retina. J. Neurosci. 16, 8041–8056 (1996).

    Article  CAS  Google Scholar 

  23. Brivanlou, I.H., Warland, D.K. & Meister, M. Mechanisms of concerted firing among retinal ganglion cells. Neuron 20, 527–539 (1998).

    Article  CAS  Google Scholar 

  24. DeVries, S.H. Correlated firing in rabbit retinal ganglion cells. J. Neurophysiol. 81, 908–920 (1999).

    Article  CAS  Google Scholar 

  25. Hu, E.H. & Bloomfield, S.A. Gap junctional coupling underlies the short-latency spike synchrony of retinal alpha ganglion cells. J. Neurosci. 23, 6768–6777 (2003).

    Article  CAS  Google Scholar 

  26. Hidaka, S., Akahori, Y. & Kurosawa, Y. Dendrodendritic electrical synapses between mammalian retinal ganglion cells. J. Neurosci. 24, 10553–10567 (2004).

    Article  CAS  Google Scholar 

  27. Wassle, H. Parallel processing in the mammalian retina. Nat. Rev. Neurosci. 5, 747–757 (2004).

    Article  Google Scholar 

  28. Chichilnisky, E.J. & Baylor, D.A. Synchronized firing by ganglion cells in monkey retina. Soc. Neurosci. Abstr. 25, 1042 (1999).

    Google Scholar 

  29. Boycott, B.B. & Wassle, H. Morphological classification of bipolar cells of the primate retina. Eur. J. Neurosci. 3, 1069–1088 (1991).

    Article  Google Scholar 

  30. de la Rocha, J., Doiron, B., Shea-Brown, E., Josic, K. & Reyes, A. Correlation between neural spike trains increases with firing rate. Nature 448, 802–806 (2007).

    Article  CAS  Google Scholar 

  31. Zaghloul, K.A., Boahen, K. & Demb, J.B. Different circuits for ON and OFF retinal ganglion cells cause different contrast sensitivities. J. Neurosci. 23, 2645–2654 (2003).

    Article  CAS  Google Scholar 

  32. Victor, J.D. & Purpura, K.P. Nature and precision of temporal coding in visual cortex: a metric-space analysis. J. Neurophysiol. 76, 1310–1326 (1996).

    Article  CAS  Google Scholar 

  33. Murphy, G.J. & Rieke, F. Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52, 511–524 (2006).

    Article  CAS  Google Scholar 

  34. Marshak, D.W., Yamada, E.S., Bordt, A.S. & Perryman, W.C. Synaptic input to an ON parasol ganglion cell in the macaque retina: a serial section analysis. Vis. Neurosci. 19, 299–305 (2002).

    Article  Google Scholar 

  35. Bordt, A.S., Hoshi, H., Yamada, E.S., Perryman-Stout, W.C. & Marshak, D.W. Synaptic input to OFF parasol ganglion cells in macaque retina. J. Comp. Neurol. 498, 46–57 (2006).

    Article  Google Scholar 

  36. Wassle, H., Grunert, U., Chun, M.H. & Boycott, B.B. The rod pathway of the macaque monkey retina: identification of AII-amacrine cells with antibodies against calretinin. J. Comp. Neurol. 361, 537–551 (1995).

    Article  CAS  Google Scholar 

  37. Hornstein, E.P., Verweij, J. & Schnapf, J.L. Electrical coupling between red and green cones in primate retina. Nat. Neurosci. 7, 745–750 (2004).

    Article  CAS  Google Scholar 

  38. Veruki, M.L. & Hartveit, E. AII (Rod) amacrine cells form a network of electrically coupled interneurons in the mammalian retina. Neuron 33, 935–946 (2002).

    Article  CAS  Google Scholar 

  39. Peichl, L., Buhl, E.H. & Boycott, B.B. Alpha ganglion cells in the rabbit retina. J. Comp. Neurol. 263, 25–41 (1987).

    Article  CAS  Google Scholar 

  40. Dacey, D.M. & Petersen, M.R. Dendritic field size and morphology of midget and parasol ganglion cells of the human retina. Proc. Natl. Acad. Sci. USA 89, 9666–9670 (1992).

    Article  CAS  Google Scholar 

  41. Chichilnisky, E.J. & Kalmar, R.S. Functional asymmetries in ON and OFF ganglion cells of primate retina. J. Neurosci. 22, 2737–2747 (2002).

    Article  CAS  Google Scholar 

  42. Schneidman, E., Bialek, W. & Berry, M.J. Synergy, redundancy and independence in population codes. J. Neurosci. 23, 11539–11553 (2003).

    Article  CAS  Google Scholar 

  43. Dunn, F.A., Doan, T., Sampath, A.P. & Rieke, F. Controlling the gain of rod-mediated signals in the mammalian retina. J. Neurosci. 26, 3959–3970 (2006).

    Article  CAS  Google Scholar 

  44. Schnapf, J.L., Nunn, B.J., Meister, M. & Baylor, D.A. Visual transduction in cones of the monkey Macaca fascicularis. J. Physiol. (Lond.) 427, 681–713 (1990).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank J. Cafaro, E.J. Chichilnisky, G. Murphy, E. Shea-Brown and J. Shlens for comments on the manuscript and for enlightening discussions; D. Carleton, E. Martinson and P. Newman for excellent technical assistance; and Dennis Dacey, Joanna Crook, Orin Packer, Toni Haun and Beth Peterson for providing primate tissue. Support was provided by the Howard Hughes Medical Institute and the US National Institutes of Health (EY-11850).

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  1. Philipp Khuc Trong

    Present address: Present address: Department of Physics, University of Technology Kaiserslautern, Kaiserslautern Rhineland-Palatinate 67653, Germany.,

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  1. Department of Physiology and Biophysics, Howard Hughes Medical Institute, University of Washington, 1959 NE Pacific Street, HSB J187, Seattle, 98195, Washington, USA

    Philipp Khuc Trong & Fred Rieke

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F.R. conducted the experiments. P.K.T. and F.R. analyzed the data and wrote the manuscript.

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Correspondence to Fred Rieke.

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Trong, P., Rieke, F. Origin of correlated activity between parasol retinal ganglion cells. Nat Neurosci 11, 1343–1351 (2008). https://doi.org/10.1038/nn.2199

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