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Synchronization of neuronal responses in the optic tectum of awake pigeons

Published online by Cambridge University Press:  02 June 2009

Sergio Neuenschwander ,
Andreas K. Engel ,
Peter König ,
Wolf Singer  and
Francisco J. Varela
Andreas K. Engel
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstraße 46, 60528 Frankfurt am Main, Germany
Peter König
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstraße 46, 60528 Frankfurt am Main, Germany
Wolf Singer
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstraße 46, 60528 Frankfurt am Main, Germany
Francisco J. Varela
Affiliation:
Max-Planck-Institut für Hirnforschung, Deutschordenstraße 46, 60528 Frankfurt am Main, Germany
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Abstract

Multiunit activity was recorded in the optic tectum of awake pigeons with two electrodes at sites varying in depth and separated by 0.3 to 3.0 mm. Autocorrelation and cross-correlation functions were computed from the recorded spike trains to determine temporal relationships in the neuronal firing patterns. Cross-correlation analysis revealed that spatially separate groups of cells in the tectum show synchronous responses to a visual stimulus. Strong synchronization occurred in both superficial and deep layers of the tectum, in general with zero-phase shift. The response synchronization in the avian optic tectum resembles that observed in the mammalian cortex, suggesting that it may subserve common functions in visual processing.

Keywords

Temporal codingSynchronizationOscillationOptic tectumPigeon
Type
Research Articles
Information
Visual Neuroscience , Volume 13 , Issue 3 , May 1996 , pp. 575 - 584
Copyright
Copyright © Cambridge University Press 1996

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References

Acheson, D.W.K., Kemplay, S.K. & Webster, K.E. (1980). Quantitative analysis of optic terminal profile distribution within the pigeon optic tectum. Neuroscience 5, 1067–1084.CrossRefGoogle ScholarPubMed
Aertsen, A.M.H.J. & Gerstein, G.L. (1985). Evaluation of neuro-nal connectivity: Sensitivity of cross-correlation. Brain Research 340, 341–354.CrossRefGoogle Scholar
Angaut, P. & RepéRant, J. (1976). Fine structure of the optic fibre termination layers in the pigeon optic tectum: A Golgi and electron microscope study. Neuroscience 1, 93–105.CrossRefGoogle ScholarPubMed
Bravo, H. & Pettigrew, J.D. (1981). The distribution of neurons projecting from the retina and visual cortex to the thalamus and tectum opticum of the barn owl, Tyto alba, and the burrowing owl, Speotyto cunicularia. Journal of Comparative Neurology 199, 419–441.CrossRefGoogle Scholar
Brecha, N., Hunt, S.P. & Karten, H.J. (1976). Relations between the optic tectum and basal ganglia in the pigeon. Society for Neuro-sciences Abstracts 2, 1069.Google Scholar
Clarke, P.G.H. & Whitteridge, D. (1976). The projection of the retina, including the red area on to the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 61, 351–358.CrossRefGoogle Scholar
Crick, F. (1984). Function of the thalamic reticular complex: The searchlight hypothesis. Proceedings of the National Academy of Sciences of the U.S.A. 81, 4586–4590.CrossRefGoogle ScholarPubMed
Damasio, A.R. (1990). Synchronous activation in multiple cortical regions: A mechanism for recall. Seminars in the Neurosciences 2, 287–296.Google Scholar
Du Lac, S. & Knudsen, E.I. (1990). Neural maps of head movement vector and speed in the optic tectum of the barn owl. Journal of Neurophysiology 63, 131–146.CrossRefGoogle ScholarPubMed
Engel, A.K., König, P., Gray, C.M. & Singer, W. (1990). Stimulus-dependent neuronal oscillations in cat visual cortex: Inter-columnar interaction as determined by cross-correlation analysis. European Journal of Neuroscience 2, 588–606.CrossRefGoogle ScholarPubMed
Engel, A.K., König, P. & Singer, W. (1991 a). Direct physiological evidence for scene segmentation by temporal coding. Proceedings of the National Academy of Sciences of the U.S.A. 88, 9136–9140.CrossRefGoogle ScholarPubMed
Engel, A.K., König, P., Kreiter, A.K. & Singer, W. (1991 b). Inter-hemispheric synchronization of oscillatory neuronal responses in cat visual cortex. Science 252, 1177–1179.CrossRefGoogle Scholar
Engel, A.K., König, P., Kreiter, A.K., Schillen, T.B. & Singer, W. (1992). Temporal coding in the visual cortex: New vistas on integration in the nervous system. Trends in Neurosciences 15, 218–226.CrossRefGoogle ScholarPubMed
Frost, B.J. & Di Franco, D.E. (1976). Motion specific units in the pigeon's optic teclum. Vision Research 16, 1229–1234.CrossRefGoogle Scholar
Frost, B.J. & Nakayama, K. (1983). Single visual neurons code opposing motion independent of direction. Science 220, 744–745.CrossRefGoogle ScholarPubMed
Frost, B.J., Cavanagh, P. & Morgan, B. (1988). Deep tectal cells in the pigeons respond to kinematograms. Journal of Comparative Physiology A 162, 639–647.CrossRefGoogle ScholarPubMed
Gerstein, G.L. (1970). Functional association of neurons: Detection and interpretation. In The Neurosciences Second Study Program, ed. Schmitt, P.O., pp. 648–661. New York: Rockefeller.Google Scholar
Glaser, E.M. & Ruchkin, D.S. (1976). Principles of Neurobiological Signal Analysis. New York: Academic Press.Google Scholar
Gochin, P.M., Miller, E.K., Gross, C.G. & Gerstein, G.L. (1991). Functional interactions among neurons in inferior temporal cortex of the awake macaque. Experimental Brain Research 84, 505–516.CrossRefGoogle ScholarPubMed
Gray, C., König, P., Engel, A.K. & Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334–337.CrossRefGoogle ScholarPubMed
Hamdi, F.A. & Whitteridge, D. (1954). The representation of the retina on the optic tectum of the pigeon. Quarterly Journal of Experimental Physiology 39, 111–119.CrossRefGoogle ScholarPubMed
Hardy, O., Leresche, N. & Jassik-Gerschenfeld, D. (1984). Post-synaptic potentials in neurons of the pigeon's optic tectum in response to afferent stimulation from the retina and other visual structures: An intracellular study. Brain Research 311, 65–74.CrossRefGoogle Scholar
Hardy, O., Leresche, N. & Jassik-Gerschenfeld, D. (1985). Morphology and laminar distribution of electrophysiologically identified cells in the pigeon's optic tectum: An intracellular study. Journal of Comparative Neurology 233, 390–404.CrossRefGoogle ScholarPubMed
Hodos, W. & Karten, H.J. (1974). Visual intensity and patterns discrimination deficits after lesions of the optic lobe in pigeons. Brain, Behavior, and Evolution 9, 165–194.Google ScholarPubMed
Hodos, W., Macko, K.A. & Bessette, B.B. (1984). Near-field acuity changes after visual system lesions in pigeons. II. Telencephalon. Behavioral Brain Research 13, 15–30.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Brecha, N. (1984). The avian tectum: A synthesis of morphology and biochemistry. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 619–648. New York: Plenum.CrossRefGoogle Scholar
Hunt, S.P. & Webster, K.E. (1975). The projection of the retina upon the optic tectum of the pigeon. Journal of Comparative Neurology 162, 433–446.CrossRefGoogle ScholarPubMed
Hunt, S.P., Streit, P., Künzle, H. & Cuénod, M. (1977). Characterization of the pigeon isthmo-tectal pathway by selective uptake and retrograde movement of radioactive compounds and by Golgi-like horseradish peroxidase labeling. Brain Research 129, 197–212.CrossRefGoogle ScholarPubMed
Jarvis, C.D. (1974). Visual discrimination and spatial localization deficits after lesions of the teclofugal pathway in pigeons. Brain, Behavior, and Evolution 9, 195–228.Google ScholarPubMed
Jassik-Gerschenfeld, D. & Hardy, O. (1984). The avian optic tectum: Neurophysiology and behavioral correlations. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 649–685. New York: Plenum.CrossRefGoogle Scholar
Karten, H.J., Hodos, W., Nauta, W.J.H. & Revzin, A.M. (1973). Neural connections of the “visual Wulst” of the avian telencephalon. Experimental studies in the pigeon (Columba livia) and owl (Speotyto cunicularia). Journal of Comparative Neurology 150, 253–278.CrossRefGoogle ScholarPubMed
König, P. (1994). A method for the quantification of synchrony and oscillatory properties of neuronal activity. Journal of Neuroscience Methods 54, 31–37.CrossRefGoogle ScholarPubMed
König, P., Engel, A.K. & Singer, W. (1995). The relation between oscillatory activity and long-range synchronization in cat visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 92, 290–294.CrossRefGoogle ScholarPubMed
Kreiter, A.K. & Singer, W. (1992). Oscillatory neuronal responses in the visual cortex of the awake monkey. European Journal of Neuroscience 4, 369–375.CrossRefGoogle Scholar
Kreiter, A.K., Engel, A.K. & Singer, W. (1992). Stimulus dependent synchronization in the caudal superior temporal sulcus of macaque monkeys. Society for Neuroscience Abstracts 18, 12.Google Scholar
Krüger, J. & Aiple, F. (1988). The connectivity underlying the orientation selectivity in the infragranular layers of monkey striate cortex. Brain Research 477, 57–65.CrossRefGoogle Scholar
Leresche, N., Hardy, O. & Jassik-Gerschenfeld, D. (1983). Receptive field properties of single cells in the pigeon's optic tectum during cooling of the visual Wulst. Brain Research 267, 225–236.CrossRefGoogle ScholarPubMed
Leresche, N., Hardy, O. & Jassik-Gerschenfeld, D. (1984). Suppressive regions in the visual receptive fields of single cells of the pigeon's optic tectum. Experimental Brain Research 53, 327–334.CrossRefGoogle ScholarPubMed
Mastronarde, D.N. (1989). Correlated firing of retinal ganglion cells. Trends in Neurosciences 12, 75–80.CrossRefGoogle ScholarPubMed
Melssen, W.J. & Epping, W.J.M. (1987). Detection and estimation of neural connectivity based on cross-correlation analysis. Biological Cybernetics 57, 403–414.CrossRefGoogle Scholar
Michalski, A., Gerstein, G.L., Czarkowska, J. & Tarnecki, R. (1983). Interactions between cat striate cortex neurons. Experimental Brain Research 51, 97–107.CrossRefGoogle ScholarPubMed
Nauta, W.J.H. & Karten, H.J. (1970). A general profile of the vertebrate brain, with sidelights on the ancestry of cerebral cortex. In The Neurosciences Second Study Program, ed. Schmitt, P.O. pp. 7–26. New York: Rockefeller.Google Scholar
Nelson, J.I., Salin, P.A., Munk, M.H.-J., Arzi, M. & Bullier, J. (1992). Spatial and temporal coherence in cortico-cortical connections: A cross-correlation study in areas 17 and 18 in the cat. Visual Neuroscience 9, 21–37.CrossRefGoogle ScholarPubMed
Neuenschwander, S. & Varela, F.J. (1992). Synchronized oscillatory activity in the optic tectum of the pigeon. Society for Neuroscience Abstracts 18, 213.Google Scholar
Neuenschwander, S. & Varela, F.J. (1993). Visually-triggered neuronal oscillations in the pigeon: An autocorrelation study of tectal activity. European Journal of Neuroscience 5, 870–881.CrossRefGoogle ScholarPubMed
Perkel, D.H., Gerstein, G.L. & Moore, G.P. (1967 a). Neuronal spike trains and stochastic point process 1. The single spike train. Biophysical Journal 7, 391–418.CrossRefGoogle Scholar
Perkel, D.H., Gerstein, G.L. & Moore, G.P. (1967 b). Neuronal spike trains and stochastic point process II. Simultaneous spike trains. Biophysical Journal 7, 419–440.CrossRefGoogle ScholarPubMed
Prechtl, J.C. (1994). Visual motion induces synchronous oscillations in turtle visual cortex. Proceedings of the National Academy of Sciences of the U.S.A. 91, 12467–12471.CrossRefGoogle ScholarPubMed
Press, W.H., Flannery, B.P., Teukolsky, S.A. & Vetterling, W.T. (1986). Numerical Recipes. Cambridge: Cambridge University Press.Google Scholar
Ramón y Cajal, S. (1911). Histologie du Système Nerveuxde l'Homme et des Vertébrés. Reed. 1952, Vol. 2, pp. 197–212. Madrid: Institute Ramón y Cajal.Google Scholar
Remy, M. & Güntürkün, O. (1991). Retinal afferents to the tectum opticum and the nucleus opticus principalis thalanii in the pigeon. Journal of Comparative Neurology 305, 57–70.CrossRefGoogle Scholar
Repérant, J. & Angaut, P. (1977). The retinotectal projections in the pigeon. An experimental optical and electron microscope study. Neuroscience 2, 119–140.CrossRefGoogle ScholarPubMed
Roelfsema, P.R., König, P., Engel, A.K., Sireteanu, R. & Singer, W. (1994). Reduced synchronization in the visual cortex of cats with strabismic amblyopia. European Journal of Neuroscience 6, 1645–1655.CrossRefGoogle ScholarPubMed
Schwarz, C. & Bolz, J. (1991). Functional specificity of a long-range horizontal connection in cat visual cortex: A cross-correlation study. Journal of Neuroscience 11, 2995–3007.CrossRefGoogle ScholarPubMed
Sejnowski, T.R. (1986). Open questions about computation in cerebral cortex. In Parallel Distributed Processing, Vol. 2, ed. Mcclelland, J.L. & Rumelhart, D.E., pp. 372–389. Cambridge: MIT Press.Google Scholar
Shimizu, T. & Karten, H.J. (1991). Central visual pathways in reptiles and birds: Evolution of the visual system. In Evolution of the Eye and the Visual System, ed. Cronly-Dillon, J.R. & Gregory, R.L., pp. 421–441. New York: Macmillan.Google Scholar
Singer, W. (1990). Search for coherence: A basic principle of cortical self-organization. Concepts in Neuroscience 1, 1–26.Google Scholar
Singer, W. (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology 55, 349–374.CrossRefGoogle ScholarPubMed
Stein, B.E. (1984). Multimodal representation in the superior colliculus and optic tectum. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 819–841. New York: Plenum.CrossRefGoogle Scholar
Stevens, J.K. & Gerstein, G.L. (1976). Interaction between cat lateral geniculate neurons. Journal of Neurophysiology 39, 239–256.CrossRefGoogle ScholarPubMed
Stone, J. & Freeman, J.A. (1971). Synaptic organization of the pigeon's optic tectum: A Golgi and current source-density analysis. Brain Research 27, 203–221.CrossRefGoogle ScholarPubMed
Toyama, K., Kimura, M. & Tanaka, K. (1981). Cross-correlation analysis of interneuronal connectivity in cat visual cortex. Journal of Neurophysiology 46, 191–201.CrossRefGoogle ScholarPubMed
Ts'O, D.Y., Gilbert, C. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6, 1160–1170.CrossRefGoogle ScholarPubMed
Von Der Malsburg, C. (1981). The Correlation Theory of Brain Function. Internal Report 81–2. Göttingen: Max-Planck-Institute for Biophysical Chemistry.Google Scholar
Zeki, S. (1993). A Vision of the Brain. Oxford: Blackwell.Google Scholar