Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T10:43:29.619Z Has data issue: false hasContentIssue false
  • English
  • Français

Principal neuronal organization in the frog optic tectum revealed by a current source density analysis

Published online by Cambridge University Press:  02 June 2009

Hideki Nakagawa ,
Hiromi Miyazaki  and
Nobuyoshi Matsumoto
Hideki Nakagawa
Affiliation:
Department of Biochemical Engineering and Science, Faculty of Computer Science and Systems Engineering, Kyushu Institute of Technology, Iizuka, Fukuoka 820, Japan
Hiromi Miyazaki
Affiliation:
Department of Biochemical Engineering and Science, Faculty of Computer Science and Systems Engineering, Kyushu Institute of Technology, Iizuka, Fukuoka 820, Japan
Nobuyoshi Matsumoto
Affiliation:
Department of Biochemical Engineering and Science, Faculty of Computer Science and Systems Engineering, Kyushu Institute of Technology, Iizuka, Fukuoka 820, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

In the frog optic tectum, the spatiotemporal pattern of neuronal activity evoked by electrical stimulation of the optic tract was examined by means of a current source density (CSD) analysis. The CSD depth profile was highly reproducible in different experiments. In all seven CSD profiles, three current sinks A, B, and D were observed in the retinorecipient layers. Four out of the seven profiles show additional two sinks C and E below the retinorecipient layers. Very small and short lasting sinks related to afferent fiber activities precede sinks A and B by about 1 ms, which could be accounted for by monosynaptic delay, in the corresponding depth region. The earliest prominent sink A at the bottom of the retinorecipient layers reflects only excitatory monosynaptic activities derived from R3 and/or R4 retinal ganglion cells. The second prominent sink B in the superficial retinorecipient layer is composed partly of excitatory monosynaptic activity from medium-sized myelinated optic fibers. It may involve excitatory monosynaptic activity from unmyelinated optic fibers and further polysynaptic activity. The fourth prominent sink D in the intermediate retinorecipient layer partially reflects excitatory monosynaptic activity derived from unmyelinated optic fibers. It may also involve further polysynaptic activity. In contrast with these three sinks, the third prominent sink C and fifth sink E exclusively reflect intratectal polysynaptic activity that has not been reported in any previous CSD studies in the frog optic tectum. These sinks almost overlap spatially in the tectal layer. We also measured the intratectal resistance changes and computed inhomogeneous CSD depth profiles to show that the results from homogeneous CSD computation assuming constant conductivity are valid for our present study. Finally, we compared the present results with previously reported CSD studies on the frog optic tectum and discuss consistencies and discrepancies among these experiments.

Keywords

Frog optic tectumCurrent source density analysisIntratectal conductivityRetinotectal connectionIntratectal connection
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 2 , March 1997 , pp. 263 - 275
Copyright
Copyright © Cambridge University Press 1997

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Antal, M, Matsumoto, N. & Székely, G. (1986). Tectal neurons of the frog: Intracellular recording and labeling with cobalt electrodes. Journal of Comparative Neurology 246, 238–253.CrossRefGoogle ScholarPubMed
Bode-Greuel, K. M., Singer, W. & Aldenhoff, J.B. (1987). A current source density analysis of field potentials evoked in slices of visual cortex. Experimental Brain Research 69, 213–219.CrossRefGoogle ScholarPubMed
Brookhart, J.M. & Fadiga, E. (1960). Potential fields initiated during monosynaptic activation of frog motoneurones. Journal of Physiology 150, 633–655.CrossRefGoogle ScholarPubMed
Cauller, L.J. & Kulics, A.T. (1988). A comparison of awake and sleeping cortical states by analysis of the somatosensory-evoked response of postcentral area 1 in rhesus monkey. Experimental Brain Research 72, 584–592.CrossRefGoogle ScholarPubMed
Chung, S.H., Bliss, T.V.P. & Keating, M.J. (1974). The synaptic organization of optic afferents in the amphibian tectum. Proceedings of the Royal Society B (London) 187, 421–447.Google ScholarPubMed
Debski, E.A. & Constantine-Paton, M. (1990). Evoked pre- and postsynaptic activity in the optic tectum of the cannulated tadpole. Journal of Comparative Physiology A 167, 377–390.CrossRefGoogle ScholarPubMed
Di, S., Baumgartner, C. & Barth, D.S. (1990). Laminar analysis of extracellular field potentials in rat vibrissa/barrel cortex. Journal of Neurophysiology 63, 832–840.CrossRefGoogle ScholarPubMed
Ewert, J.-P. (1984). Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 247–416. New York and London: Plenum Press.CrossRefGoogle Scholar
Freeman, B. & Singer, W. (1983). Direct and indirect visual inputs to superficial layers of cat superior colliculus: A current source-density analysis of electrically evoked potentials. Journal of Neurophysiology 49, 1075–1091.CrossRefGoogle ScholarPubMed
Freeman, J.A. & Nicholson, C. (1975). Experimental optimization of current source-density technique for anuran cerebellum. Journal of Neurophysiology 38, 369–382.CrossRefGoogle ScholarPubMed
Freeman, J.A. (1977). Possible regulatory function of acetylcholine receptor in maintenance of retinotectal synapses. Nature 269, 218–222.CrossRefGoogle ScholarPubMed
Freeman, J. A., Schmidt, J.T. & Oswald, R.E. (1980). Effect of α-bungarotoxin on retinotectal synaptic transmission in the goldfish and the toad. Neuroscience 5, 929–942.CrossRefGoogle ScholarPubMed
Freygang, W.H. Jr & Landau, W.M. (1955). Some relations between resistivity and electrical activity in the cerebral cortex of the cat. Journal of Cellular and Comparative Physiology 45, 377–392.CrossRefGoogle ScholarPubMed
Fujita, Y. & Sakata, H. (1962). Electrophysiological properties of CA1 and CA2 apical dendrites of rabbit hippocampus. Journal of Neurophysiology 25, 209–222.CrossRefGoogle ScholarPubMed
Gaze, R.M. & Keating, M.J. (1968). The depth distribution of visual units in the tectum of the frog following regeneration of the optic nerve. Journal of Physiology 200, 128–129.Google Scholar
George, S.A. & Marks, W.B. (1974). Optic nerve terminal arborizations in the frog: Shape and orientation inferred from electrophysiological measurements. Experimental Neurology 42, 467–482.CrossRefGoogle ScholarPubMed
Givre, S. J., Arezzo, J.C. & Schroeder, C.E. (1995). Effects of wavelength on the timing and laminar distribution of illuminance-evoked activity in macaque VI. Visual Neuroscience 12, 229–239.CrossRefGoogle Scholar
Grant, A.C. & Lettvin, J.Y. (1991). Sources of electrical transients in tectal neuropil of the frog, Ranapipiens. Brain Research 560, 106–121.CrossRefGoogle Scholar
Grüsser, O.-J. & Grüsser-Cornehls, U. (1976). Neurophysiology of the anuran visual system. In Frog Neurobiology, ed. Llinás, R. & Precht, W., pp. 297–385. Berlin, Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Haberly, L.B. & Shepherd, G.M. (1973). Current-density analysis of summed evoked potentials in opossum prepyriform cortex. Journal of Neurophysiology 36, 789–802.CrossRefGoogle ScholarPubMed
Häusser, M., Stuart, G., Racca, C. & Sakmann, B. (1995). Axonal initiation and active dendritic propagation of action potentials in substantia nigra neurons. Neuron 15, 637–647.CrossRefGoogle ScholarPubMed
Hickmott, P.W. & Constantine-Paton, M. (1993). The contributions of NMDA, Non-NMDA, and GABA receptors to postsynaptic responses in neurons of the optic tectum. Journal of Neuroscience 13, 4339–4353.CrossRefGoogle ScholarPubMed
Holsheimer, J. (1987). Electrical conductivity of the hippocampal CA1 layers and application to current-source-density analysis. Experimental Brain Research 67, 402–410.CrossRefGoogle ScholarPubMed
Hughes, T.E. (1990). A light- and electron-microscopic investigation of the optic tectum of the frog, Rana pipiens, I: The retinal axons. Visual Neuroscience 4, 499–518.CrossRefGoogle ScholarPubMed
Kenan-Vaknin, G. & Teyler, T.J. (1994). Laminar pattern of synaptic activity in rat primary visual cortex: Comparison of in vivo and in vitro studies employing the current source density analysis. Brain Research 635, 37–48.CrossRefGoogle ScholarPubMed
Knudsen, E.I. & Brainard, M.S. (1995). Creating a unified representation of visual and auditory space in the brain. Annual Review of Neuro-science 18, 19–43.CrossRefGoogle ScholarPubMed
Lázár, G.Y. & Széely, G.Y. (1969). Distribution of optic terminals in the different optic centres of the frog. Brain Research 16, 1–14.CrossRefGoogle ScholarPubMed
Lázár, G.Y., Tóth, P., Csank, G.Y. & Kicliter, E. (1983). Morphology and location of tectal projection neurons in frogs: A study with HRP and cobalt-filling. Journal of Comparative Neurology 215, 108–120.CrossRefGoogle ScholarPubMed
Lettvin, J.Y., Maturana, H.R., McCulloch, W.S. & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of the Institute of Radio Engineers of New York 47, 1940–1951.Google Scholar
Llinás, R., Nicholson, C, Freeman, J.A. & Hillman, D.E. (1968). Dendritic spikes and their inhibition in alligator Purkinje cells. Science 160, 1132–1135.CrossRefGoogle ScholarPubMed
Luhmann, H.J., Greuel, J.M. & Singer, W. (1990). Horizontal interactions in cat striate cortex: II. A current source-density analysis. European Journal of Neuroscience 2, 358–368.CrossRefGoogle Scholar
Matsumoto, N. & Bando, T. (1980). Excitatory synaptic potentials and morphological classification of tectal neurons of the frog. Brain Research 192, 39–48.CrossRefGoogle ScholarPubMed
Matsumoto, N., Schwippert, W.W. & Ewert, J.-P. (1986). Intracellular activity of morphologically identified neurons of the grass frog's optic tectum in response to moving configurational visual stimuli. Journal of Comparative Physiology A 159, 721–739.CrossRefGoogle Scholar
Maturana, H.R., Lettvin, J.Y., McCulloch, W.S. & Pitts, W.H. (1960). Anatomy and physiology of vision in the frog (Rana pipiens). Journal of General Physiology 43, 129–175.CrossRefGoogle Scholar
Mitzdorf, U. & Singer, W. (1977). Laminar segregation of afferents to lateral geniculate nucleus of the cat: An analysis of current source density. Journal of Neurophysiology 40, 1227–1244.CrossRefGoogle Scholar
Mitzdorf, U. & Singer, W. (1978). Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): Acurrent source density analysis of electrically evoked potentials. Experimental Brain Research 33, 371–394.CrossRefGoogle Scholar
Mitzdorf, U. & Singer, W. (1979). Excitatory synaptic ensemble properties in the visual cortex of the macaque monkey: A current source density analysis of electrically evoked potentials. Journal of Comparative Neurology 187, 71–84.CrossRefGoogle ScholarPubMed
Mitzdorf, U. & Singer, W. (1980). Monocular activation of visual cortex in normal and monocularly deprived cats: An analysis of evoked potentials. Journal of Physiology 304, 203–220.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1985). Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiological Reviews 65, 37–100.CrossRefGoogle ScholarPubMed
Mitzdorf, U. (1986). The physiological causes of VEP: Current source density analysis of electrically and visually evoked potentials. In Evoked Potentials, ed. Cracco, R.Q. & Bodis-Wolliner, I., pp. 141–154. New York: Alan R. Liss.Google Scholar
Nakagawa, H., Kikkawa, S. & Matsumoto, N. (1994). Synaptic connection patterns between frog retinal ganglion cells and tectal neurons revealed by whole-cell recordings in vivo. Brain Research 665, 319–322.CrossRefGoogle ScholarPubMed
Nicholson, C. (1973). Theoretical analysis of field potentials in anisotropic ensembles of neuronal elements. IEEE Transactions on Biomedical Engineering BME-20, 278–288.CrossRefGoogle ScholarPubMed
Nicholson, C. & Freeman, J.A. (1975). Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. Journal of Neurophysiology 38, 356–368.CrossRefGoogle ScholarPubMed
Potter, H.D. (1969). Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiand). Journal of Comparative Neurology 136, 203–232.CrossRefGoogle Scholar
Rappelsberger, P., Pockberger, H. & Petsche, H. (1981). Current source density analysis: Methods and application to simultaneously recorded field potentials of the rabbit's visual cortex. Pflügers Archiv 389, 159–170.CrossRefGoogle ScholarPubMed
Rodriguez, R. & Haberly, L.B. (1989). Analysis of synaptic events in the opossum piriform cortex with improved current source-density techniques. Journal of Neurophysiology 61, 702–718.CrossRefGoogle ScholarPubMed
Scalia, F. (1973). Autoradiographic demonstration of optic nerve fibers in the stratum zonale of the frog's tectum. Brain Research 58, 484–488.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
SzékelyY, G. & Lázár, G. (1976). Cellular and synaptic architecture of the optic tectum. In Frog Neurobiology, ed. Llinás, R. & Precht, W., pp. 407–434. Berlin, Heidelberg, New York: Springer Verlag.CrossRefGoogle Scholar
Vaknin, G., DiScenna, P.G. & Teyler, T.J. (1988). A method for calculating current source density (CSD) analysis without resorting to recording sites outside the sampling volume. Journal of Neuroscience Methods 24, 131–135.CrossRefGoogle ScholarPubMed
Vanegas, H., Williams, B. & Freeman, J.A. (1979). Responses to stimulation of marginal fibers in the teleostean optic tectum. Experimental Brain Research 34, 335–349.CrossRefGoogle ScholarPubMed
Witpaard, J. & Keurs, H.E.D.J. ter (1975). A reclassification of retinal ganglion cells in the frog, based upon tectal endings and response properties. Vision Research 15, 1333–1338.CrossRefGoogle ScholarPubMed