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. 2011 Oct 6;2(9):764–771. doi: 10.1007/s13238-011-1091-5

Spikes with short inter-spike intervals in frog retinal ganglion cells are more correlated with their adjacent neurons’ activities

Wen-Zhong Liu 1, Ru-Jia Yan 1, Wei Jing 1, Hai-Qing Gong 1, Pei-Ji Liang 1,✉
PMCID: PMC4875263  PMID: 21976066

Abstract

Correlated firings among neurons have been extensively investigated; however, previous studies on retinal ganglion cell (RGC) population activities were mainly based on analyzing the correlated activities between the entire spike trains. In the present study, the correlation properties were explored based on burst-like activities and solitary spikes separately. The results indicate that: (1) burst-like activities were more correlated with other neurons’ activities; (2) burst-like spikes correlated with their neighboring neurons represented a smaller receptive field than that of correlated solitary spikes. These results suggest that correlated burst-like spikes should be more efficient in signal transmission, and could encode more detailed spatial information.

Keywords: correlated firing, burst-like spikes, solitary spikes, correlation index, receptive field

References

  1. Barlow H.B. The Ferrier Lecture, 1980. Critical limiting factors in the design of the eye and visual cortex. Proc R Soc Lond B Biol Sci. 1981;212:1–34. doi: 10.1098/rspb.1981.0022. [DOI] [PubMed] [Google Scholar]
  2. Bloomfield S.A., Völgyi B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat Rev Neurosci. 2009;10:495–506. doi: 10.1038/nrn2636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brivanlou I.H., Warland D.K., Meister M. Mechanisms of concerted firing among retinal ganglion cells. Neuron. 1998;20:527–539. doi: 10.1016/S0896-6273(00)80992-7. [DOI] [PubMed] [Google Scholar]
  4. Chen A.H., Zhou Y., Gong H.Q., Liang P.J. Firing rates and dynamic correlated activities of ganglion cells both contribute to retinal information processing. Brain Res. 2004;1017:13–20. doi: 10.1016/j.brainres.2004.04.081. [DOI] [PubMed] [Google Scholar]
  5. DeVries S.H. Correlated firing in rabbit retinal ganglion cells. J Neurophysiol. 1999;81:908–920. doi: 10.1152/jn.1999.81.2.908. [DOI] [PubMed] [Google Scholar]
  6. Field G., Chichilnisky E. Information processing in the primate retina: circuitry and coding. Annu Rev Neurosci. 2007;30:1–30. doi: 10.1146/annurev.neuro.30.051606.094252. [DOI] [PubMed] [Google Scholar]
  7. Field G.D., Sher A., Gauthier J.L., Greschner M., Shlens J., Litke A.M., Chichilnisky E.J. Spatial properties and functional organization of small bistratified ganglion cells in primate retina. J Neurosci. 2007;27:13261–13272. doi: 10.1523/JNEUROSCI.3437-07.2007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Hirsch J.A., Alonso J.M., Reid R.C., Martinez L.M. Synaptic integration in striate cortical simple cells. J Neurosci. 1998;18:9517–9528. doi: 10.1523/JNEUROSCI.18-22-09517.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ishikane H., Gangi M., Honda S., Tachibana M. Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nat Neurosci. 2005;8:1087–1095. doi: 10.1038/nn1497. [DOI] [PubMed] [Google Scholar]
  10. Jin X., Chen A.H., Gong H.Q., Liang P.J. Information transmission rate changes of retinal ganglion cells during contrast adaptation. Brain Res. 2005;1055:156–164. doi: 10.1016/j.brainres.2005.07.006. [DOI] [PubMed] [Google Scholar]
  11. Jing W., Liu W.Z., Gong X.W., Gong H.Q., Liang P.J. Influence of GABAergic inhibition on concerted activity between the ganglion cells. Neuroreport. 2010;21:797–801. doi: 10.1097/WNR.0b013e32833c5b50. [DOI] [PubMed] [Google Scholar]
  12. Jing W., Liu W.Z., Gong X.W., Gong H.Q., Liang P.J. Visual pattern recognition based on spatio-temporal patterns of retinal ganglion cells’ activities. Cogn Neurodynamics. 2010;4:179–188. doi: 10.1007/s11571-010-9119-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lettvin J., Maturana H., McCulloch W., Pitts W. What the frog’s eye tells the frog’s brain. Proc IRE. 1959;47:1940–1951. doi: 10.1109/JRPROC.1959.287207. [DOI] [Google Scholar]
  14. Li Y., Li H., Gong H.Q., Liang P.J., Zhang P.M. Characteristics of receptive field encoded by synchronized firing pattern of ganglion cell group. Acta Biophys Sin. 2011;03:211–221. doi: 10.3724/SP.J.1260.2011.00211. [DOI] [Google Scholar]
  15. Lisman J.E. Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci. 1997;20:38–43. doi: 10.1016/S0166-2236(96)10070-9. [DOI] [PubMed] [Google Scholar]
  16. Liu W.Z., Jing W., Li H., Gong H.Q., Liang P.J. Spatial and temporal correlations of spike trains in frog retinal ganglion cells. J Comput Neurosci. 2011;30:543–553. doi: 10.1007/s10827-010-0277-9. [DOI] [PubMed] [Google Scholar]
  17. Meister M. Multineuronal codes in retinal signaling. Proc Natl Acad Sci U S A. 1996;93:609–614. doi: 10.1073/pnas.93.2.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Meister M., Lagnado L., Baylor D.A. Concerted signaling by retinal ganglion cells. Science. 1995;270:1207–1210. doi: 10.1126/science.270.5239.1207. [DOI] [PubMed] [Google Scholar]
  19. Meister M., Pine J., Baylor D.A. Multi-neuronal signals from the retina: acquisition and analysis. J Neurosci Methods. 1994;51:95–106. doi: 10.1016/0165-0270(94)90030-2. [DOI] [PubMed] [Google Scholar]
  20. Neuenschwander S., Singer W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature. 1996;379:728–732. doi: 10.1038/379728a0. [DOI] [PubMed] [Google Scholar]
  21. Pillow J.W., Shlens J., Paninski L., Sher A., Litke A.M., Chichilnisky E.J., Simoncelli E.P. Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature. 2008;454:995–999. doi: 10.1038/nature07140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rowe M.H., Fischer Q. Dynamic properties of retinogeniculate synapses in the cat. Vis Neurosci. 2001;18:219–231. doi: 10.1017/S0952523801182076. [DOI] [PubMed] [Google Scholar]
  23. Schneidman E., Berry M.J., 2nd, Segev R., Bialek W. Weak pairwise correlations imply strongly correlated network states in a neural population. Nature. 2006;440:1007–1012. doi: 10.1038/nature04701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schnitzer M.J., Meister M. Multineuronal firing patterns in the signal from eye to brain. Neuron. 2003;37:499–511. doi: 10.1016/S0896-6273(03)00004-7. [DOI] [PubMed] [Google Scholar]
  25. Schwartz G., Taylor S., Fisher C., Harris R., Berry M.J., 2nd Synchronized firing among retinal ganglion cells signals motion reversal. Neuron. 2007;55:958–969. doi: 10.1016/j.neuron.2007.07.042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shlens J., Rieke F., Chichilnisky E. Synchronized firing in the retina. Curr Opin Neurobiol. 2008;18:396–402. doi: 10.1016/j.conb.2008.09.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sincich L.C., Adams D.L., Economides J.R., Horton J.C. Transmission of spike trains at the retinogeniculate synapse. J Neurosci. 2007;27:2683–2692. doi: 10.1523/JNEUROSCI.5077-06.2007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Snider R.K., Kabara J.F., Roig B.R., Bonds A.B. Burst firing and modulation of functional connectivity in cat striate cortex. J Neurophysiol. 1998;80:730–744. doi: 10.1152/jn.1998.80.2.730. [DOI] [PubMed] [Google Scholar]
  29. Usrey W.M., Reppas J.B., Reid R.C. Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature. 1998;395:384–387. doi: 10.1038/26487. [DOI] [PubMed] [Google Scholar]
  30. Usrey W.M., Reppas J.B., Reid R.C. Specificity and strength of retinogeniculate connections. J Neurophysiol. 1999;82:3527–3540. doi: 10.1152/jn.1999.82.6.3527. [DOI] [PubMed] [Google Scholar]
  31. Wang Y., Pang J., Lin L. Multi-channel in vivo recording in brain of freely behaving rats. Acta Biophys Sin. 2010;26:397–405. [Google Scholar]
  32. Yang W., Li Y., Li B., Tian X. Time-varying spectrum synchronous pattern and behavior-event encoding by multichannel local field potentials. Acta Biophys Sin. 2010;26:225–233. [Google Scholar]
  33. Zhang P.M., Wu J.Y., Zhou Y., Liang P.J., Yuan J.Q. Spike sorting based on automatic template reconstruction with a partial solution to the overlapping problem. J Neurosci Methods. 2004;135:55–65. doi: 10.1016/j.jneumeth.2003.12.001. [DOI] [PubMed] [Google Scholar]

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