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Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae

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Summary

Tongue-projecting plethodontid salamanders have massive direct ipsilateral retinal afferents to the tectum opticum as well as a large and well developed nucleus isthmi. Retrograde staining revealed two subnuclei: A ventral one projecting to the contralateral tectal hemisphere and a dorsal one projecting back to the ipsilateral side. The isthmic nuclei show a retinotopic organization, which is in register with that of the tectum. Electrophysiological recordings from nucleus-isthmi neurons revealed response properties that are very similar to those found in tectal neurons. Thus, there is no substantial processing of tectal neural activity in the nucleus isthmi. Measurements of peak latencies after electrical and light stimulation suggest the continuous coexistence of 4 representations of the visual field in the tectum mediated by (1) the contralateral and (2) the ipsilateral direct retinal afferents, (3) the uncrossed and (4) the crossed isthmo-tectal projection. (1) and (2) originate at the same moment in the retina and arrive simultaneously in the tectum. It is assumed that in plethodontid salamanders with massive ipsilateral retino-tectal projections depth perception based on disparity cues is achieved by comparison of these images.

Representations mediated by (3) and (4) arriving in the tectum at the same time as (1) and (2) originate 10–30 ms earlier in the retina. It is hypothesized that these time differences between (1)/(2) and (3)/(4) are used to calculate three-dimensional trajectories of fast-moving prey objects.

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Abbreviations

EL :

edge length

FDA :

fluoresceine dextranamine

RDA :

tetramethylrhodamine dextranamine

RF :

receptive field

References

  • Adams JC (1981) Heavy metal intensification of DAB-based HRP-reaction product. J Histochem Cytochem 29:775

    Google Scholar 

  • Antal M, Matsumoto N, Székely G (1986) Tectal neurons of the frog: Intracellular recording and labeling with cobalt electrodes. J Comp Neurol 246:238–253

    Google Scholar 

  • Caine HS, Gruberg ER (1985) Ablation of nucleus isthmi leads to loss of specific visually elicited behaviors in the frog Rana pipiens. Neurosci Lett 54:307–312

    Google Scholar 

  • Chung SH, Bliss TVP, Keating MJ (1974) The synaptic organization of optic afferents in the amphibian tectum. Proc R Soc Lond B 187:421–447

    Google Scholar 

  • Collett TS (1977) Stereopsis in toads. Nature 267:349–351

    Google Scholar 

  • Collett TS, Udin SB, Finch DJ (1987) A possible mechanism for binocular depth judgements in anurans. Exp Brain Res 66:35–40

    Google Scholar 

  • Dann JF, Beazley LD (1982) The development of connections between the isthmic nucleus and the tectum in Xenopus and Limnodynastes tadpoles. Neurosci Lett 33:107–113

    Google Scholar 

  • Fisher MD, Udin SB (1988) Connections between the nucleus isthmi and the tectum in larval and post-metamorphic axolotls. J Neurobiol 19:111–125

    Google Scholar 

  • Fite KV, Scalia F (1976) Central visual pathways in the frog. In: Fite KV (ed) The amphibian visual system. A multidisciplinary approach. Academic Press, London New York, pp 87–118

    Google Scholar 

  • Fritzsch B (1980) Retinal projections in European Salamandridae. Cell Tissue Res 213:325–341

    Google Scholar 

  • Gaillard F (1985) Binocularly driven neurons in the rostral part of the frog optic tectum. J Comp Physiol A 157:47–55

    Google Scholar 

  • Gimlich RL, Braun J (1985) Improved fluorescent compounds for tracing cell lineage. Dev Biol 109:509–514

    Google Scholar 

  • Glasser S, Ingle D (1978) The nucleus isthmus as a relay station in the ipsilateral visual projection to the frog's optic tectum. Brain Res 159:214–218

    Google Scholar 

  • Graybiel AM (1978) A satellite system of the superior colliculus: The parabigeminal nucleus and its projections to the superficial collicular layers. Brain Res 145:365–374

    Google Scholar 

  • Grobstein P, Comer C (1983) The nucleus isthmi as an intertectal relay for the ipsilateral oculotectal projection in the frog, Rana pipiens. J Comp Neurol 217:54–74

    Google Scholar 

  • Grobstein P, Comer C, Hollyday M, Archer SM (1978) A crossed isthmo-tectal projection in Rana pipiens and its involvement in the ipsilateral visuotectal projection. Brain Res 156:117–123

    Google Scholar 

  • Gruberg ER, Harris WA (1981) The serotonergic somatosensory projection to the tectum of normal and eyeless salamanders. J Morphol 170:55–69

    Google Scholar 

  • Gruberg ER, Lettvin J (1980) Anatomy and physiology of a binocular system in the frog Rana pipiens. Brain Res 192:313–325

    Google Scholar 

  • Gruberg ER, Udin SB (1978) Topographic projections between the nucleus isthmi and the tectum of the frog Rana pipiens. J Comp Neurol 179:487–500

    Google Scholar 

  • Grüsser OJ, Grüsser-Cornehls U (1976) Neurophysiology of the anuran visual system. In: Llinas R, Precht W (eds) Frog neurobiology. Springer, Berlin Heidelberg New York, pp 297–385

    Google Scholar 

  • Herrick CJ (1948) The brain of the tiger salamander Ambystoma tigrinum. The University of Chicago Press, Chicago

    Google Scholar 

  • Jordan M, Luthardt G, Meyer-Naujoks C, Roth G (1980) The role of eye accommodation in the depth perception of common toads. Z Naturforsch 35c:851–852

    Google Scholar 

  • Keating MJ, Gaze RM (1970) The ipsilateral retinotectal pathway in the frog. J Exp Physiol 55:284–292

    Google Scholar 

  • Künzle H, Schnyder H (1984) The isthmus-tegmentum complex in the turtle and rat: A comparative analysis of its interconnections with the optic tectum. Exp Brain Res 56:509–522

    Google Scholar 

  • Larsell O (1967) The comparative anatomy and histology of the cerebellum from myxinoids through birds. University of Minnesota Press, Minneapolis

    Google Scholar 

  • Linden R, Perry VH (1983) Retrograde and anterograde transneuronal degeneration in the parabigeminal nucleus following tectal lesions in developing rats. J Comp Neurol 218:270–281

    Google Scholar 

  • Linke R, Roth G (1988) Neuroglial cells and axons in the optic nerve of lungless salamanders (Fam. Plethodontidae) In: Elsner N, Barth FG (eds) Sense organs. Thieme, Stuttgart, p 255

    Google Scholar 

  • Linke R, Roth G (1990) Optic nerves in plethodontid salamanders (Amphibia, Urodela): neuroglia, fiber spectrum and myelination. Anat Embryol 181:37–48

    Google Scholar 

  • Lombard RE, Wake DB (1976) Tongue evolution in the lungless salamanders, family Plethodontidae I. Introduction, theory and a general model of dynamics. J Morphol 148:265–286

    Google Scholar 

  • Lombard RE, Wake DB (1977) Tongue evolution in the lungless salamanders, family Plethodontidae II. Function and evolutionary diversity. J Morphol 153:39–79

    Google Scholar 

  • Luthardt-Laimer G (1981) Distance estimation in binocular and monocular salamanders. Z Tierpsychol 63:233–240

    Google Scholar 

  • Manteuffel G, Fox B, Roth G (1989) Topographic relationships of ipsi- and contralateral visual inputs to the rostral tectum opticum in the salamander Plethodon jordani indicate the presence of a horopter. Neurosci Lett 107:105–109

    Google Scholar 

  • Martinez S, Puelles L (1988) Avian nucleus isthmi ventralis projects to the contralateral optic tectum. Brain Res 481:181–184

    Google Scholar 

  • Naujoks-Manteuffel C, Manteuffel G (1988) Origins of descending projections to the medulla oblongata and rostral medulla spinalis in the urodele Salamandra salamandra (Amphibia). J Comp Neurol 273:187–206

    Google Scholar 

  • Northcutt RG (1982) Localization of neurons afferent to the optic tectum in longnose gars. J Comp Neurol 204:325–335

    Google Scholar 

  • Opdam P, Nieuwenhuys R (1976) Topological analysis of the brain stem of the axolotl Ambystoma mexicanum. J Comp Neurol 165:285–306

    Google Scholar 

  • Rettig G (1984) Neuroanatomische Untersuchungen der visuellen Projektionen bei Salamandern (Ordnung Caudata). Diss Univ Bremen

  • Rettig G (1988) Connections of the tectum opticum in two urodeles, Salamandra salamandra and Bolitoglossa subpalmata, with special reference to the nucleus isthmi. J Hirnforsch 29:5–16

    Google Scholar 

  • Rettig G, Roth G (1982) Afferent visual projections in three species of lungless salamanders (Family Plethodontidae). Neurosci Lett 31:221–224

    Google Scholar 

  • Rettig G, Roth G (1986) Retinofugal projections in salamanders of the family Plethodontidae. Cell Tissue Res 243:285–296

    Google Scholar 

  • Roldan M, Reinoso-Suárez F, Tortelly A (1983) Parabigeminal projections to the superior colliculus in the cat. Brain Res 280:1–13

    Google Scholar 

  • Roth G (1976) Experimental analysis of the prey catching behavior of Hydromantes italicus Dunn (Amphibia, Plethodontidae). J Comp Physiol 109:47–58

    Google Scholar 

  • Roth G (1982) Beuteerkennungsmechanismen im Tectum opticum von Amphibien — eine vergleichende Untersuchung. Funkt Biol Med 1:90–98

    Google Scholar 

  • Roth G (1982) Responses in the optic tectum of the salamander Hydromantes italicus to moving prey stimuli. Exp Brain Res 45:386–392

    Google Scholar 

  • Roth G (1987) Visual behavior in salamanders. Springer, Berlin

    Google Scholar 

  • Roth G, Naujoks-Manteuffel C, Grunwald W (1990) Cytoarchitecture of the tectum mesencephali in salamanders: A Golgi and HRP study. J Comp Neurol 291:27–42

    Article  Google Scholar 

  • Sakamoto N, Ito H, Ueda S (1981) Topographic projections between the nucleus isthmi and the optic tectum in a teleost, Navodon modes tus. Brain Res 224:225–234

    Google Scholar 

  • Sereno MI, Ulinski PS (1987) Caudal topographic nucleus isthmi and the rostral nontopographic nucleus isthmi in the turtle, Pseudemys scripta. J Comp Neurol 261:319–346

    Google Scholar 

  • Thexton AJ, Wake DB, Wake MH (1977) Tongue function in the salamander Bolitoglossa occidentalis. Arch Oral Biol 22:361–366

    Google Scholar 

  • Udin SB (1987) A projection from the mesencephalic tegmentum to the nucleus isthmi in the frogs, Rana pipiens and Acris crepitons. Neuroscience 21:631–637

    Google Scholar 

  • Udin SB, Fisher MD (1985) The development of the nucleus isthmi in Xenopus laevis I. Cell genesis and the formation of connections with the tectum. J Comp Neurol 232:25–35

    Google Scholar 

  • Wang S, Yan K, Wang Y (1980) Visual field topography and binocular responses in frog's nucleus isthmi. Scientia Sinica Vol XXIV No 9:1292–1301

    Google Scholar 

  • Wang S, Yan K, Wang Y (1981) Visual field topography in the frog's nucleus isthmi. Neurosci Lett 23:37–41

    Google Scholar 

  • Wang S, Yan K, Wang Y (1982) Nucleus isthmus of toad is secondary visual center. Scientia Sinica Vol XXV No 11:1172–1178

    Google Scholar 

  • Wang S, Yan K, Wang Y, Jiang S, Wang X (1983) Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Res 275:355–360

    Google Scholar 

  • Welker E, Hoogland PV, Lohman AHM (1983) Tectal connections in Python reticulatus. J Comp Neurol 220:347–354

    Google Scholar 

  • Wiggers W (1991) Elektrophysiologische, neuroanatomische und verhaltensphysiologische Untersuchungen zur visuellen Verhaltenssteuerung bei lungenlosen Salamandern. Diss Universität Bremen

  • Wilczynski W, Northcutt RG (1977) Afferents to the optic tectum of the leopard frog: An HRP study. J Comp Neurol 173:219–230

    Google Scholar 

Download references

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  1. Institut für Hirnforschung, Universität Bremen, W-2800, Bremen 33, FRG

    Wolfgang Wiggers & Gerhard Roth

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  1. Wolfgang Wiggers
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  2. Gerhard Roth
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Wiggers, W., Roth, G. Anatomy, neurophysiology and functional aspects of the nucleus isthmi in salamanders of the family Plethodontidae. J Comp Physiol A 169, 165–176 (1991). https://doi.org/10.1007/BF00215863

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