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Organization of ascending projections from the optic tectum and mesencephalic pretectal gray in Rana pipiens

Published online by Cambridge University Press:  02 June 2009

Neil M. Montgomery  and
Katherine V. Fite
Neil M. Montgomery
Affiliation:
Neuroscience and Behavior Program, University of Massachusetts, Amherst
Katherine V. Fite
Affiliation:
Neuroscience and Behavior Program, University of Massachusetts, Amherst
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Abstract

The ascending projections from the dorsal mesencephalon to the thalamus and pretectum in Rana pipiens were investigated by using the anterograde and retrograde transport of HRP with regard to two major issues:

(1) the degree of tectotopic organization in the projections, and (2) their cells of origin.

The results indicate that the spatial organization of the tecto-thalamic tract is specifically related to the laminar organization of the contributing tectal efferent neurons. Axons of neurons in the superficial portion of tectal layer 8 exit the tectum through layer 9 and travel in the superficial portion of the dorsal and ventral tecto-thalamic tracts and innervate the nucleus lentiformis mesencephali, the posterior lateral dorsal nucleus, and corpus geniculatum. The distribution of terminals within these structures varied with the tectal HRP-injection site. HRP injections in the ventral tecto-thalamic tract retrogradely labeled neurons in the superficial portion of tectal layer 8 across the lateral and caudal portion of the tectal lobe. HRP injections into the dorsal tecto-thalamic tract, at the level of the pretectum, retrogradely labeled pyriform neurons in the superficial portion of tectal layer 8 in the rostral and medial portions of the tectal lobe.

With regard to the deep tectal layers, axons from pyramidal neurons in layer 6 and ganglionic neurons in layer 8 leave the tectum through layer 7, travel in both the dorsal and ventral tecto-thalamic tracts, and are located internal to the axons of the pyriform neurons of superficial tectal layer 8. The majority of the ganglionic neurons project to the posterior lateral ventral nucleus and the anterior lateral nucleus. The distribution of terminals within these nuclei did not display a tectotopic organization.

A second major projection to the thalamus originates from the mesencephalic pretectal gray and innervates the nucleus lentiformis mesencephali, the posterior lateral dorsal nucleus, the anterior lateral nucleus, dorsal and ventral divisions of the ventral lateral thalamus, and the nucleus of Bellonci. Other axons from the mesencephalic pretectal gray terminate in the contralateral, medial portions of the posterior lateral dorsal thalamus, the ventral lateral thalamus, and the anterior lateral nucleus.

The isthmo-tectal projection was also retrogradely labeled following tectal injections of HRP. This pathway travels in the most ventral portion of the ventral tecto-thalamic tract; its axons passed over the lateral margin of the endopeduncular nucleus bilaterally, and crossed the midline in the caudal portion of the optic chiasm. Extensive, bead-like varicosities were observed on these axons both in the endopeduncular nucleus and in the posterior optic chiasm.

These results, taken together with those from other species, strongly suggest that a common organizational plan exists among terrestrial vertebrates with regard to the specific pattern of innervation of pretectal and thalamic nuclei by either the optic tectum or the superior colliculus.

Keywords

Tectothalamic tractRetinotopic organizationPretectumSubcortical visionAmphibian visual system
Type
Research Articles
Information
Visual Neuroscience , Volume 7 , Issue 5 , November 1991 , pp. 459 - 478
Copyright
Copyright © Cambridge University Press 1991

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References

Ariens-Kappers, C.U., Huber, G.C. & Crosby, E.C. (1936). The Comparative Anatomy of the Nervous System of Vertebrates, Including Man. New York, MacMillian.Google Scholar
Benevento, L.A. & Standage, G. (1983). The organization of projections of the retino-recipient and nonretino-recipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307–336.CrossRefGoogle Scholar
Benowitz, L.A. & Karten, H.J. (1976). Organization of tectofugal pathways in the pigeon: a retrograde-transport study. Journal of Comparative Neurology 167, 503–520.CrossRefGoogle Scholar
Corvaja, N. & D'Ascanio, P. (1981). Spinal projections from the mesencephalon in the toad. Brain, Behavior, and Evolution 19, 205–213.CrossRefGoogle ScholarPubMed
Dacey, D. & Ulinski, P.S. (1983). Nucleus rotundus in a snake (Thamnophis siralis): an analysis of a nonretinotopic projection. Journal of Comparative Neurology 216, 175–191.CrossRefGoogle Scholar
Dacey, D. & Ulinski, P.S. (1986). Optic tectum of the eastern garter snake (Thamnophis siralis), I: Efferent pathways. Journal of Comparative Neurology 245, 1–28.CrossRefGoogle Scholar
Ebbesson, S.O.E. (1970). Selective silver impregnation of degenerating axoplasm in poikilothermic vertebrates. In Contemporary Research Methods in Neuroanatomy, ed. Nauta, W.J.H. & Ebbesson, S.O.E., pp. 132–161. Berlin Heidelberg, New York: Springer-Verlag.CrossRefGoogle Scholar
Ebbesson, S.O.E. (1972). A proposal for a common nomenclature for some optic nuclei in vertebrates and evidence for a common origin of two such cell groups. Brain, Behavior, and Evolution 6, 92–130.CrossRefGoogle ScholarPubMed
Ewert, J.P. (1986). DerEinflub von Zwischenhirndefekten auf die Visuomotorik im Beute- und Fluchtverhalten der Erdkrote (Bufo bufo L). Zeitschrift für Vergleichende Physiologie 61, 41–70.CrossRefGoogle Scholar
Ewert, J.P. (1971). Single-unit of the toad (Bufo americanus) caudal thalamus to visual objects. Zeitschrift für Vergleichende Physiologie 74, 81–102.CrossRefGoogle Scholar
Ewert, J.P. & Borchers, H.W. (1971). Reaktionscharakteristik von Neuronen aus dem Tectum opticum und subtectum der Erdkrote (Bufo bufo L). Zeitschrift für Vergleichende Physiologie 71, 165–189.CrossRefGoogle Scholar
Fite, K.V. & Scalia, F. (1976). Central visual pathways in the frog. In The Amphibian Visual System ed. Fite, K.V. pp. 87–118. New York: Academic Press.CrossRefGoogle Scholar
Foster, R.F. & Hall, W.C. (1975). The connections and laminar organization of the optic tectum in a reptile (Inguana iguana). Journal of Comparative Neurology 163, 397–426.CrossRefGoogle Scholar
Gaupp, E. (1899). A Ecker's and R. Wiedersheim's Anatomie des Frosches, Zweite Abteilung. Lehre vom Nervensystem, E. Vieweg, Braunschweig.Google Scholar
Graham, J. & Casagrande, V.A. (1980). A light-microscopic and electron-microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). Journal of Comparative Neurology 191, 133–151.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1973). The thalamocortical projections of the so-called posterior nuclear group: a study with anterograde degeneration methods in the cat. Brain Research 49, 229–244.CrossRefGoogle Scholar
Grover, B.G. & Sharma, S.C. (1979). Tectal projections in the gold-fish (Carassius auratus): a degeneration study. Journal of Comparative Neurology 184, 435–451.CrossRefGoogle Scholar
Gruberg, E., Wallace, M. & Waldeck, R. (1989). Relationship between isthmotectal fibers and other tectopetal systems in the leopard frog. Journal of Comparative Neurology 288, 39–50.CrossRefGoogle ScholarPubMed
Hanker, J.Yates, P., Metz, C. & Rustioni, A. (1977). A new specific, sensitive, and noncarcinogenic reagent for the demonstration of horseradish peroxidase. Journal of Histochemistry 9, 789–792.CrossRefGoogle ScholarPubMed
Hunt, S.P. & Kunzle, H. (1976). Selective uptake and transport of label within three identified neuronal systems after injection of [3H]-GABA in the pigeon optic tectum: an autoradiographic study. Journal of Comparative Neurology 170, 173–190.CrossRefGoogle Scholar
Hunt, S.P., Streit, P., Kunzle, H. & Cuenod, M. (1977). Characterization of the pigeon isthmc-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
Hutchins, B. & Updyke, B.V. (1989). Retinotopic organization within the lateral posterior complex of the cat. Journal of Comparative Neurology 285, 350–398.CrossRefGoogle ScholarPubMed
Katz, M.J. & Lasek, R. (1981). Substrate pathways demonstrated by transplanted Mauthner axons. Journal of Comparative Neurology 195, 627–641.CrossRefGoogle ScholarPubMed
Lazar, G. (1969). Efferent projections of the optic tectum in the frog. Acta Biologica Academiae Scientiarum Hungaricae 20, 171–183.Google Scholar
Lazar, 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 ScholarPubMed
Gros-Clark, W.E.Le (1933). The medial geniculate and nucleus isthmi. Journal of Anatomy 67, 536–548.Google Scholar
Masino, T. & Grobstein, P. (1990). Tectal connectivity in the frog (Rana pipiens): Tectotegmental projections and general analysis of topographic organization. Journal of Comparative Neurology 291, 103–127.CrossRefGoogle ScholarPubMed
Montgomery, N. & Fite, K. (1989). Retinotopic organization of central optic projections in Rana pipiens. Journal of Comparative Neurology 283, 526–540.CrossRefGoogle ScholarPubMed
Montgomery, N. (1989). Somatomotor connectivity in the midbrain of Rana pipiens. Brain, Behavior, and Evolution 34, 96–109.CrossRefGoogle ScholarPubMed
Montgomery, N.M. & Mergandalh, R. (1989). The tecto-thalamic tract in a type 2 lizard: cells of origin and evidence for topography. Neuroscience Abstracts 15, 1392.Google Scholar
Neary, T.J. & Northcutt, R.G. (1983). Nuclear organization of the bullfrog diencephalon. Journal of Comparative Neurology 213, 262–278.CrossRefGoogle ScholarPubMed
Parent, A. (1976). Striatial afferent connections in the turtle (Chrysemys picta) as revealed by retrograde axonal transport of horseradish peroxidase. Brain Research 108, 25–36.CrossRefGoogle Scholar
Rubinson, K. (1968). Projections of the tectum opticum of the leopard frog. Brain, Behavior, and Evolution 1, 529–561.CrossRefGoogle Scholar
Sefton, A.J. & Martin, P.R. (1984). Relation of the parabigeminal nucleus to the superior colliculus and dorsal lateral geniculate nucleus in the hooded rat. Experimental Brain Research 56, 144–148.CrossRefGoogle Scholar
Sterling, R. & Merrill, E. (1987). Functional morphology of frog retinal ganglion cells and their central projections: the dimming detector. Journal of Comparative Neurology 258, 477–495.CrossRefGoogle Scholar
Wilczynski, W. & Northcutt, R.G. (1977). Afferents to the optic tectum of the leopard frog: an HRP study. Journal of Comparative Neurology 173, 219–229.CrossRefGoogle Scholar
Wilczynski, W. & Northcutt, R.G. (1983). Connections of the bull-frog striatum: afferent organization. Journal of Comparative Neurology 214, 321–332.CrossRefGoogle Scholar
Wild, M. (1989). Pretectal and tectal projections to the homologue of the dorsal lateral genicuate nucleus in the pigeon: an anterograde and retrograde-tracing study with cholera toxin conjugated to horse-radish peroxidase. Brain Research 479, 130–137.CrossRefGoogle Scholar