Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Synchronized retinal oscillations encode essential information for escape behavior in frogs

Nature Neuroscience volume 8, pages 1087–1095 (2005)Cite this article

Abstract

Synchronized oscillatory activity is generated among visual neurons in a manner that depends on certain key features of visual stimulation. Although this activity may be important for perceptual integration, its functional significance has yet to be explained. Here we find a very strong correlation between synchronized oscillatory activity in a class of frog retinal ganglion cells (dimming detectors) and a well-known escape response, as shown by behavioral tests and multi-electrode recordings from isolated retinas. Escape behavior elicited by an expanding dark spot was suppressed and potentiated by intraocular injection of GABAA receptor and GABAC receptor antagonists, respectively. Changes in escape behavior correlated with antagonist-evoked changes in synchronized oscillatory activity but not with changes in the discharge rate of dimming detectors. These antagonists did not affect the expanding dark spot–induced responses in retinal ganglion cells other than dimming detectors. Thus, synchronized oscillations in the retina are likely to encode escape-related information in frogs.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Bicuculline suppressed escape behavior in response to the expanding dark spot.
Figure 2: Effects of bicuculline on the activities of retinal ganglion cells.
Figure 3: Spike trains evoked by an expanding dark spot in multiple dimming detectors in the isolated retina.
Figure 4: Bicuculline impaired the synchronized oscillations among dimming detectors.
Figure 5: Effects of bicuculline on synchronization and oscillations.
Figure 6: Effects of a GABACR antagonist on escape behavior and the activities of retinal ganglion cells.
Figure 7: TPMPA enhanced the synchronized oscillatory activity among dimming detectors.
Figure 8: Effects of GABAR antagonists on optokinetic responses.

Similar content being viewed by others

References

  1. Eckhorn, R. et al. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol. Cybern. 60, 121–130 (1988).

    Article  CAS  PubMed  Google Scholar 

  2. Gray, C.M., König, P., Engel, A.K. & Singer, W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337 (1989).

    Article  CAS  PubMed  Google Scholar 

  3. Wehr, M. & Laurent, G. Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384, 162–166 (1996).

    Article  CAS  PubMed  Google Scholar 

  4. Fries, P., Roelfsema, P.R., Engel, A.K., König, P. & Singer, W. Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. Proc. Natl. Acad. Sci. USA 94, 12699–12704 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Stopfer, M., Bhagavan, S., Smith, B.H. & Laurent, G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70–74 (1997).

    Article  CAS  PubMed  Google Scholar 

  6. Laurent, G. A systems perspective on early olfactory coding. Science 286, 723–728 (1999).

    Article  CAS  PubMed  Google Scholar 

  7. Rodriguez, E. et al. Perception's shadow: long-distance synchronization of human brain activity. Nature 397, 430–433 (1999).

    Article  CAS  PubMed  Google Scholar 

  8. Castelo-Branco, M., Goebel, R., Neuenschwander, S. & Singer, W. Neural synchrony correlates with surface segregation rules. Nature 405, 685–689 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Patel, A.D. & Balaban, E. Temporal patterns of human cortical activity reflect tone sequence structure. Nature 404, 80–84 (2000).

    Article  CAS  PubMed  Google Scholar 

  10. Engel, A.K., Fries, P. & Singer, W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2, 704–716 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Engel, A.K. & Singer, W. Temporal binding and the neural correlates of sensory awareness. Trends Cogn. Sci. 5, 16–25 (2001).

    Article  PubMed  Google Scholar 

  12. Fell, J. et al. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci. 4, 1259–1264 (2001).

    Article  CAS  PubMed  Google Scholar 

  13. Fries, P., Reynolds, J.H., Rorie, A.E. & Desimone, R. Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291, 1560–1563 (2001).

    Article  CAS  PubMed  Google Scholar 

  14. Neuenschwander, S. & Singer, W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature 379, 728–733 (1996).

    Article  CAS  PubMed  Google Scholar 

  15. Castelo-Branco, M., Neuenschwander, S. & Singer, W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J. Neurosci. 18, 6395–6410 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Gray, C.M. & Singer, W. Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci. USA 86, 1698–1702 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Engel, A.K., Kreiter, A.K., König, P. & Singer, W. Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. Proc. Natl. Acad. Sci. USA 88, 6048–6052 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Engel, A.K., König, P., Kreiter, A.K. & Singer, W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252, 1177–1179 (1991).

    Article  CAS  PubMed  Google Scholar 

  19. Engel, A.K., König, P. & Singer, W. Direct physiological evidence for scene segmentation by temporal coding. Proc. Natl. Acad. Sci. USA 88, 9136–9140 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kreiter, A.K. & Singer, W. Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey. J. Neurosci. 16, 2381–2396 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Engel, A.K., König, P., Kreiter, A.K., Schillen, T.B. & Singer, W. Temporal coding in the visual cortex: new vistas on integration in the nervous system. Trends Neurosci. 15, 218–226 (1992).

    Article  CAS  PubMed  Google Scholar 

  22. Singer, W. & Gray, C.M. Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555–586 (1995).

    Article  CAS  PubMed  Google Scholar 

  23. Waldeck, R.F. & Gruberg, E.R. Studies on the optic chiasm of the leopard frog. I. Selective loss of visually elicited avoidance behavior after optic chiasm hemisection. Brain Behav. Evol. 46, 84–94 (1995).

    Article  CAS  PubMed  Google Scholar 

  24. King, J.G., Lettvin, J.Y. & Gruberg, E.R. Selective, unilateral, reversible loss of behavioral responses to looming stimuli after injection of tetrodotoxin or cadmium chloride into the frog optic nerve. Brain Res. 841, 20–26 (1999).

    Article  CAS  PubMed  Google Scholar 

  25. Lettvin, J.Y., Maturana, H.R., McCulloch, W.S. & Pitts, W.H. What the frog's eye tells the frog's brain. Proc. Inst. Radio Eng. 47, 1940–1951 (1959).

    Google Scholar 

  26. Ishikane, H., Kawana, A. & Tachibana, M. Short- and long-range synchronous activities in dimming detectors of the frog retina. Vis. Neurosci. 16, 1001–1014 (1999).

    Article  CAS  PubMed  Google Scholar 

  27. Arai, I., Yamada, Y., Asaka, T. & Tachibana, M. Light-evoked oscillatory discharges in retinal ganglion cells are generated by rhythmic synaptic inputs. J. Neurophysiol. 92, 715–725 (2004).

    Article  PubMed  Google Scholar 

  28. Bäckström, A.C., Hemilä, S. & Reuter, T. Directional selectivity and colour coding in the frog retina. Med. Biol. 56, 72–83 (1978).

    PubMed  Google Scholar 

  29. 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  PubMed  Google Scholar 

  30. Dong, C.J. & Werblin, F.S. Temporal contrast enhancement via GABAC feedback at bipolar terminals in the tiger salamander retina. J. Neurophysiol. 79, 2171–2180 (1998).

    Article  CAS  PubMed  Google Scholar 

  31. Matsui, K., Hasegawa, J. & Tachibana, M. Modulation of excitatory synaptic transmission by GABAC receptor-mediated feedback in the mouse inner retina. J. Neurophysiol. 86, 2285–2298 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Bonaventure, N., Wioland, N. & Jardon, B. Anisotropic inhibition in the receptive field surround of the frog retinal ganglion cells, evidenced by bicuculline and SR 95103, a new GABA antagonist. Eur. J. Pharmacol. 121, 327–336 (1986).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  34. König, P., Engel, A.K. & Singer, W. Relation between oscillatory activity and long-range synchronization in cat visual cortex. Proc. Natl. Acad. Sci. USA 92, 290–294 (1995).

    Article  PubMed  PubMed Central  Google Scholar 

  35. Watanabe, S., Koizumi, A., Matsunaga, S., Stocker, J.W. & Kaneko, A. GABA-Mediated inhibition between amacrine cells in the goldfish retina. J. Neurophysiol. 84, 1826–1834 (2000).

    Article  CAS  PubMed  Google Scholar 

  36. Shields, C.R. & Lukasiewicz, P.D. Spike-dependent GABA inputs to bipolar cell axon terminals contribute to lateral inhibition of retinal ganglion cells. J. Neurophysiol. 89, 2449–2458 (2003).

    Article  CAS  PubMed  Google Scholar 

  37. Wässle, H., Koulen, P., Brandstätter, J.H., Fletcher, E.L. & Becker, C.M. Glycine and GABA receptors in the mammalian retina. Vision Res. 38, 1411–1430 (1998).

    Article  PubMed  Google Scholar 

  38. Du, J.L. & Yang, X.L. Subcellular localization and complements of GABAA and GABAC receptors on bullfrog retinal bipolar cells. J. Neurophysiol. 84, 666–676 (2000).

    Article  CAS  PubMed  Google Scholar 

  39. Vitanova, L. et al. Immunocytochemical and electrophysiological characterization of GABA receptors in the frog and turtle retina. Vision Res. 41, 691–704 (2001).

    Article  CAS  PubMed  Google Scholar 

  40. Grüsser, O.J. & Grüsser-Cornehls, U. Neurophysiology of the anuran visual system. in Frog Neurobiology (eds. Llinás, R. & Precht, W.) 297–385 (Springer, Berlin, 1976).

    Chapter  Google Scholar 

  41. König, P., Engel, A.K. & Singer, W. Integrator or coincidence detector? The role of the cortical neuron revisited. Trends Neurosci. 19, 130–137 (1996).

    Article  PubMed  Google Scholar 

  42. Salinas, E. & Sejnowski, T.J. Impact of correlated synaptic input on output firing rate and variability in simple neuronal models. J. Neurosci. 20, 6193–6209 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Perez-Orive, J., Bazhenov, M. & Laurent, G. Intrinsic and circuit properties favor coincidence detection for decoding oscillatory input. J. Neurosci. 24, 6037–6047 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Hutcheon, B. & Yarom, Y. Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216–222 (2000).

    Article  CAS  PubMed  Google Scholar 

  45. Grüsser, O.J. & Grüsser-Cornehls, U. Comparative physiology of movement-detecting neuronal systems in lower vertebrates (Anura and Urodela). Bibl. Ophthalmol. 82, 260–273 (1972).

    PubMed  Google Scholar 

  46. Molotchnikoff, S., Shumikhina, S. & Moisan, L.E. Stimulus-dependent oscillations in the cat visual cortex: differences between bar and grating stimuli. Brain Res. 731, 91–100 (1996).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank L.H. Pinto, T. Takahashi, I. Arai and J. Hasegawa for discussion and comments and Y. Horiuchi for excellent technical assistance. This work was supported by Grant-in-Aid for Scientific Research (12053212 and 17022014 to M.T., 14710040 and 17730424 to H.I., 1610444 to M.G.) and the Special Coordination Funds for Promoting Science and Technology (The Neuroinformatics Research in Vision Project to M.T.) from the Ministry of Education, Science, Sports and Culture. M.G. is a research fellow of the Japan Society for Promotion of Science.

Author information

Author notes

  1. Hiroshi Ishikane

    Present address: Laboratory for Neuroinformatics, RIKEN Brain Science Institute, 2-1 Hirosawa, Wako-shi, Saitama, 351-0198, Japan

Authors and Affiliations

  1. Department of Psychology, Graduate School of Humanities and Sociology, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Hiroshi Ishikane, Mie Gangi, Shoko Honda & Masao Tachibana

Authors
  1. Hiroshi Ishikane
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mie Gangi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shoko Honda
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Masao Tachibana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Masao Tachibana.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Fig. 1

Effects of expanding stimuli on escape behavior and ganglion cell activities. (PDF 502 kb)

Supplementary Fig. 2

Variation of spike discharges. (PDF 169 kb)

Supplementary Fig. 3

Dependence of the oscillatory activities of dimming detectors on the speed and final size of the expanding dark spot. (PDF 427 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ishikane, H., Gangi, M., Honda, S. et al. Synchronized retinal oscillations encode essential information for escape behavior in frogs. Nat Neurosci 8, 1087–1095 (2005). https://doi.org/10.1038/nn1497

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn1497

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing