Summary
Injections of horseradish peroxidase, wheat germ agglutinin and various amino acids into the optic tectum in both the turtle and rat, and into the nucleus isthmi magnocellularis (IsM) in the turtle were used to analyse the connections of the isthmustegmentum complex. The connectivities and the selective retrograde transport properties in certain tectal pathways were taken as a basis to define more accurately isthmus-tegmentum complex subdivisions. There were several main findings. In the turtle the projection from the tectum to the IsM originated in the stratum griseum periventriculare, whereas the projection from the IsM to the tectum terminated in the superficial tectal layers (both projections homolateral). The terminations of the pathway from IsM to tectum were not uniformly distributed throughout the tectal surface; rather, alternating zones of high and low termination density along the lateral dimension were observed. The turtle nucleus isthmi parvocellularis, receiving a few tectal fibers and afferents from the ipsilateral IsM, gave rise to a bilateral tectal projection. Evidence was obtained for a crossed collicular projection to the rat parabigeminal nucleus (Pbg) in addition to the established uncrossed one. GABA was retrogradely transported from the optic tectum to the Pbg in the rat, and to the dorsolateral mesencephalic tegmentum and the IsM in the turtle. After glycine injections into the optic tectum, the dorsomedial peri-parabigeminal tegmentum was retrogradely labeled in the rat, and the IsM in the turtle. An attempt was made to outline the parallelism between the organizations of the isthmustegmentum complexes in the turtle, pigeon and rat. It was concluded that some basic features in the inter-connectivity of the isthmus-tegmentum complex and other parts of the visual system have been preserved in evolution, despite the apparent loss of the isthmoretinal projection in mammals.
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Abbreviations
- AIO:
-
accessory isthmooptic cells
- Cbl:
-
cerebellum
- CoS:
-
superior colliculus
- Imc/Ipc:
-
n. isthmi magno-/parvocellularis
- ION:
-
n. isthmoopticus
- IsM/IsP:
-
n. isthmi magno-/parvocellularis
- LLd:
-
n. lemnisci lateralis, pars dorsali
- MeVe:
-
mesencephalic periventricular gray
- Om:
-
nucleus oculomotorius
- om:
-
nervus oculomotorius
- OT:
-
optic tectum
- PAG:
-
periaqueductal gray
- Pbg:
-
n. parabigeminalis
- PoG:
-
pontine nuclei
- SLu:
-
n. semilunaris
- TgIsLD/LV:
-
lateral isthmic tegmentum, pars dorsalis/ventralis
- TgLD/LV:
-
lateral (peri-parabigeminal) tegmentum p. dorsalis/ventralis
- TgMeDL/DM:
-
dorsolateral mesencephalic tegmentum p. lateralis/medialis
- TgMeV:
-
ventral mesencephalic tegmentum
- To:
-
nucleus trochlearis
- to:
-
nervus trochlearis
- TS:
-
Torus semicircularis
References
Baleydier C, Magnin M (1979) Afferent and efferent connections of the parabigeminal nucleus in cat revealed by retrograde axonal transport of horseradish peroxidase. Brain Res 161: 187–198
Bass AH, Northcutt RG (1981) Retinal recipient nuclei in the painted turtle Chrysemys picta: An autoradiographic and HRP study. J Comp Neurol 199: 97–112
Brecha NC (1978) Some observations on the organization of the avian optic tectum: Afferent nuclei and their tectal projections. Thesis, State University of New York, Stony Brook
Crossland WJ, Hughes CP (1978) Observations on the afferent and efferent connections of the avian isthmo-optic nucleus. Brain Res 145: 239–256
Cruce WLR, Nieuwenhuys R (1974) The cell masses in the brain stem of the turtle Testudo hermanni; a topographical and topological analysis. J Comp Neurol 156: 277–306
Foster RE, Hall WC (1975) The connections and laminar organization of the optic tectum in a reptile (Iguana iguana). J Comp Neurol 163: 397–426
Gerfen CR, O'Leary DDM, Cowan WM (1982) A note on the transneuronal transport of wheat germ agglutinin-conjugated horseradish peroxidase in the avian and rodent visual system. Exp Brain Res 48: 443–448
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
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
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
Gruberg ER, Lettvin JY (1980) Anatomy and physiology of a binocular system in the frog Rana pipiens. Brain Res 192: 313–325
Harting JK, Huerta MF, Frankfurter AJ, Storminger NL, Royce GJ (1980) Ascending pathways from the monkey superior colliculus: An autoradiographic analysis. J Comp Neurol 192: 853–882
Holcombe V, Hall WC (1981) Course and laminar origin of the tectoparabigeminal pathway. Brain Res 211: 405–411
Holstege G, Collewijn H (1982) The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J Comp Neurol 209: 139–175
Huber GC, Crosby EC (1933) The reptilian optic tectum. J Comp Neurol 57: 57–163
Hunt SP, Künzle H (1976) Observations on the projections and intrinsic organization of the pigeon optic tectum. An autoradiographic study based on anterograde and retrograde, axonal and dendritic flow. J Comp Neurol 170: 153–172
Hunt SP, 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 Res 129: 197–212
Ito H, Sakamoto N, Takatsuji K (1982) Cytoarchitecture, fiber connections and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from the optic tectum and nucleus pretectalis. J Comp Neurol 205: 299–311
Jungherr E (1945) Certain nuclear groups of the avian mesencephalon. J Comp Neurol 82: 55–76
Künzle H, Schnyder H (1983) Do retinal and spinal projections overlap within the turtle thalamus? Neuroscience 10: 161–168
LeGros Clark WE (1933) The medial geniculate and the nucleus isthmi. J Anat 67: 536–548
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
Mendez-Otero R, Rocha-Miranda CE, Perry VH (1980) The organization of the parabigemino-tectal projections in the opossum. Brain Res 198: 183–189
Mesulam MM (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: A non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26: 106–117
O'Leary DDM, Cowan WM (1982) Further studies on the development of the isthmo-optic nucleus with special reference to the occurrence and fate of ectopic and ipsilaterally projecting neurons. J Comp Neurol 212: 399–416
Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. Academic Press, Sydney, New York
Ramon P (1896) Estructura de encéfalo del camaleon. Rev Trimest Micrograf 1: 46–82
Reiner A, Brauth SE, Kitt CA, Karten HJ (1980) Basal ganglionic pathways to the optic tectum: Studies in reptiles. J Comp Neurol 193: 565–589
Roldan M, Reinoso-Suarez F, Tortelly A (1983) Parabigeminal projections to the superior colliculus in the cat. Brain Res 280: 1–13
Sanes JR, Cheney JM (1982) Lectin binding reveals a synapse-specific carbohydrate in skeletal muscle. Nature 300: 646–647
Schnyder H, Künzle H (1983a) Differential labeling in neuronal tracing with wheat germ agglutinin. Neurosci Lett 35: 115–120
Schnyder H, Künzle H (1983b) The retinopetal system in the turtle Pseudemys scripta elegans. Cell Tiss Res 234: 219–224
Schnyder H, Künzle H (1984) Is there a retinopetal system in the rat? Exp Brain Res 56: 502–508
Sherk H (1979a) A comparison of visual-response properties in cat's parabigeminal nucleus and superior colliculus. J Neurophysiol 42: 1640–1655
Sherk H (1979b) Connections and visual-field mapping in cat's tectoparabigeminal circuit. J Neurophysiol 42: 1656–1668
Stevenson JA, Lund RD (1982) Alterations of crossed parabigeminotectal projection induced by neonatal eye removal in rats. J Comp Neurol 207: 191–202
Stöckel K, Schwab M, Thoenen H (1977) Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin. Brain Res 132: 273–285
Streit P, Knecht E, Cuénod M (1979) Transmitter-specific retrograde labeling in the striato-nigral and raphe-nigral pathways. Science 205: 306–308
Udin SB (1983) Abnormal visual input leads to development of abnormal axon trajectories in frogs. Nature 301: 336–338
Wang SR, Yan K, Wang YT, Jiang SY, Wang XS (1983) Neuroanatomy and electrophysiology of the lacertilian nucleus isthmi. Brain Res 275: 355–360
Watanabe K, Kawana E (1979) Efferent projections of the parabigeminal nucleus in rats: A horseradish peroxidase (HRP) study. Brain Res 168: 1–12
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Supported by the Swiss National Science Foundation (grants no. 3.433.78, 3.505.79 and 3.580.79), the EMDO-Stiftung and the Dr. Eric Slack-Gyr-Stiftung in Zürich
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Künzle, H., Schnyder, H. 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 (1984). https://doi.org/10.1007/BF00237992
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DOI: https://doi.org/10.1007/BF00237992