Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-23T11:17:34.977Z Has data issue: false hasContentIssue false
  • English
  • Français

Current source density analysis of contra- and ipsilateral isthmotectal connections of the frog

Published online by Cambridge University Press:  04 October 2006

NORIAKI HOSHINO ,
KAZUYA TSURUDOME ,
HIDEKI NAKAGAWA  and
NOBUYOSHI MATSUMOTO
NORIAKI HOSHINO
Affiliation:
Kyushu Institute of Technology, Graduate School of Life Science and Systems Engineering, Department of Brain Science and Engineering, Wakamatsu-ku, Kitakyushu, Fukuoka, Japan
KAZUYA TSURUDOME
Affiliation:
Kyushu Institute of Technology, Graduate School of Life Science and Systems Engineering, Department of Brain Science and Engineering, Wakamatsu-ku, Kitakyushu, Fukuoka, Japan
HIDEKI NAKAGAWA
Affiliation:
Kyushu Institute of Technology, Graduate School of Life Science and Systems Engineering, Department of Brain Science and Engineering, Wakamatsu-ku, Kitakyushu, Fukuoka, Japan
NOBUYOSHI MATSUMOTO
Affiliation:
Kyushu Institute of Technology, Graduate School of Life Science and Systems Engineering, Department of Brain Science and Engineering, Wakamatsu-ku, Kitakyushu, Fukuoka, Japan
Get access Rights & Permissions [Opens in a new window]

Abstract

The nucleus isthmi (NI) of the frog receives input from the ipsilateral optic tectum and projects back to both optic tecta. After ablation of NI, frogs display no visually elicited prey-catching or threat avoidance behavior. Neural mechanisms that underlie the loss of such important behavior have not been solved. Electrophysiological examination of the contralateral isthmotectal projection has proved that it contributes to binocular vision. On the other hand, there are very few physiological investigations of the ipsilateral isthmotectal projection. In this study, current source density (CSD) analysis was applied to contra- and ipsilateral isthmotectal projections. The contralateral projection produced monosynaptic sinks in superficial layers and in layer 8. The results confirmed former findings obtained by single unit recordings. The ipsilateral projection elicited a prominent monosynaptic sink in layer 8. Recipient neurons were located in layers 6–7. These results, combined with those from the former intracellular study, led to the following neuronal circuit. Afferents from the ipsilateral NI inhibit non-efferent pear shaped neurons in the superficial layers, and strongly excite large ganglionic neurons projecting to the descending motor regions. Thus feedback to the output neurons strengthens the visually elicited responses.

Keywords

Current source density (CSD) analysisNuclear isthmiIsthmotectal projectionOptic tectumFrog
Type
Research Article
Information
Visual Neuroscience , Volume 23 , Issue 5 , September 2006 , pp. 713 - 719
Copyright
2006 Cambridge University Press

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 Scholar
Caine, H.S. & Gruberg, E.R. (1985). Ablation of nucleus isthmi leads to loss of specific visually elicited behaviors in the frog Rana pipiens. Neuroscience Letters 54, 307–312.CrossRefGoogle Scholar
Dudkin, E.A. & Gruberg, E.R. (1999). Relative number of cells projecting from contralateral and ipsilateral nucleus isthmi to loci in the optic tectum is dependent on visuotopic location: Horseradish peroxidase study in the leopard frog. Journal of Comparative Neurology 414, 212–216.3.0.CO;2-#>CrossRefGoogle Scholar
Dudkin, E.A. & Gruberg, E.R. (2003). Nucleus isthmi enhances calcium influx into optic nerve fiber terminals in Rana pipiens. Brain Research 969, 44–52.CrossRefGoogle Scholar
Freeman, J.A., Schmidt, J.T., & Oswald, R.E. (1980). Effect of alpha-bungarotoxin on retinotectal synaptic transmission in the goldfish and the toad. Neuroscience 5, 929–942.CrossRefGoogle Scholar
Gaillard, F. (1985). Binocularly driven neurons in the rostral part of the frog optic tectum. Journal of Comparative Physiology A 157, 47–55.CrossRefGoogle Scholar
Gaze, R.M. (1962). The projection of the binocular visual field on the optic tecta of the frog. Quarterly Journal of Experimental Physiology 47, 273–280.CrossRefGoogle Scholar
Gaze, R.M. & Keating, M.J. (1967). Visual responses from ipsilateral tectal units in the frog. Journal of Physiology 192, 52P–53P.Google Scholar
Gaze, R.M. & Keating, M.J. (1970). Receptive field properties of single units from the visual projection to the ipsilateral tectum in the frog. Quarterly Journal of Experimental Physiology and Cognate Medical Sciences 55, 143–152.CrossRefGoogle Scholar
George, S.A., Wu, G.Y., Li, W.C., & Wang, S.R. (1999). Dual actions of isthmic input to tectal neurons in a reptile, Gekko gekko. Visual Neuroscience 16, 889–893.Google Scholar
Grobstein, P., Comer, C., Hollyday, M., & Archer, S.M. (1978). A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Research 156, 117–123.CrossRefGoogle Scholar
Gruberg, E.R., Hughes, T.E., & Karten, H.J. (1994). Synaptic interrelationships between the optic tectum and the ipsilateral nucleus isthmi in Rana pipiens. Journal of Comparative Neurology 339, 353–364.CrossRefGoogle Scholar
Gruberg, E.R. & Lettvin, J.Y. (1980). Anatomy and physiology of a binocular system in the frog Rana pipiens. Brain Research 192, 313–325.CrossRefGoogle Scholar
Gruberg, E.R. & Udin, S.B. (1978). Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. Journal of Comparative Neurology 179, 487–500.CrossRefGoogle Scholar
Gruberg, E.R., Wallace, M.T., Caine, H.S., & Mote, M.I. (1991). Behavioral and physiological consequences of unilateral ablation of the nucleus isthmi in the leopard frog. Brain Behavior and Evolution 37, 92–103.Google Scholar
Grüsser, O. & Grüsser-Cornehls, U. (1976). Neurophysiology of the anuran visual system. In Frog Neurobiology, ed. Llinás, W. & Precht, W., pp. 297–385. Berlin: Springer.CrossRef
Guedes, R.C., Tsurudome, K., & Matsumoto, N. (2005). Spreading depression in vivo potentiates electrically-driven responses in frog optic tectum. Brain Research, 1036, 109–114.CrossRefGoogle Scholar
Khalil, S.H. & Lázár, G. (1977). Nucleus isthmi of the frog: Structure and tecto-isthmic projection. Acta Morphologica Academiae Scientiarum Hungaricae 25, 51–59.Google Scholar
Lázár, G., Toth, P., Csank, G., & 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 Scholar
Lettvin, J.Y., Maturana, W.S., McCulloch, W.S., & Pitts, W.H. (1959). What the frog's eye tells the frog's brain. Proceedings of Institute of Radio Engineers 47, 1940–1951.CrossRefGoogle Scholar
Li, Z. & Fite, K.V. (1998). Distribution of GABA-like immunoreactive neurons and fibers in the central visual nuclei and retina of frog, Rana pipiens. Visual Neuroscience 15, 995–1006.Google Scholar
Li, Z. & Fite, K.V. (2001). GABAergic visual pathways in the frog Rana pipiens. Visual Neuroscience 18, 457–464.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 Scholar
Matsumoto, N., Schwippert, 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 159, 721–739.CrossRefGoogle Scholar
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.Google Scholar
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.
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.Google Scholar
Mitzdorf, U. & Singer, W. (1978). Prominent excitatory pathways in the cat visual cortex (A 17 and A 18): A current source density analysis of electrically evoked potentials. Experimental Brain Research 33, 371–394.Google Scholar
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 Scholar
Nakagawa, H. & Matsumoto, N. (1998). ON and OFF channels of the frog optic tectum revealed by current source density analysis. Journal of Neurophysiology 80, 1886–1899.Google Scholar
Nakagawa, H., Miyazaki, H., & Matsumoto, N. (1997). Principal neuronal organization in the frog optic tectum revealed by a current source density analysis. Visual Neuroscience 14, 263–275.CrossRefGoogle Scholar
Nicholson, C. (1973). Theoretical analysis of field potentials in anisotropic ensembles of neuronal elements. IEEE Transactions on Biomedical Engineering 20, 278–288.CrossRefGoogle Scholar
Potter, H.D. (1969). Structural characteristics of cell and fiber populations in the optic tectum of the frog (Rana catesbeiana). Journal of Comparative Neurology 136, 203–231.CrossRefGoogle Scholar
Sargent, P.B., Pike, S.H., Nadel, D.B., & Lindstrom, J.M. (1989). Nicotinic acetylcholine receptor-like molecules in the retina, retinotectal pathway, and optic tectum of the frog. Journal of Neuroscience 9, 565–573.Google Scholar
Székely, G. & Lázár, G. (1976). Cellular and synaptic architecture of the optic tectum. In Frog Neurobiology, ed. Llinás, W. & Precht, W., pp. 407–457. Berlin: Springer.CrossRef
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.Google Scholar
Wang, S.R. (2003). The nucleus isthmi and dual modulation of the receptive field of tectal neurons in non-mammals. Brain Research Reviews 41, 13–25.CrossRefGoogle Scholar
Wang, S.R. & Matsumoto, N. (1990). Postsynaptic potentials and morphology of tectal cells responding to electrical stimulation of the bullfrog nucleus isthmi. Visual Neuroscience 5, 479–488.CrossRefGoogle Scholar