Hostname: page-component-848d4c4894-4hhp2 Total loading time: 0 Render date: 2024-05-20T06:16:37.147Z Has data issue: false hasContentIssue false
  • English
  • Français

Projections of the nucleus of the optic tract to the nucleus reticularis tegmenti pontis and prepositus hypoglossi nucleus in the pigmented rat as demonstrated by anterograde and retrograde transport methods

Published online by Cambridge University Press:  02 June 2009

Barbara G. Korp ,
Robert H. I. Blanks  and
Yasuhiro Torigoe
Barbara G. Korp
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine
Robert H. I. Blanks
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine Department of Surgery, Division of Otolaryngology-Head and Neck Surgery, University of California, Irvine
Yasuhiro Torigoe
Affiliation:
Department of Anatomy and Neurobiology, University of California, Irvine Department of Surgery, Division of Otolaryngology-Head and Neck Surgery, University of California, Irvine
Get access Rights & Permissions [Opens in a new window]

Abstract

The visual pathways from the nucleus of the optic tract (NOT) to the nucleus reticularis tegmenti pontis (NRTP) and prepositus hypoglossi nucleus (ph) were studied following injections of tritiated leucine into the NOT of pigmented rats. The cell bodies of origin of the pretectal-NRTP, NRTP-ph, and pretectal-ph projections were determined using retrograde horseradish peroxidase (HRP) technique.

The pretectum projects strongly to the rostral two-thirds of the central and pericentral subdivisions of the NRTP and sends a remarkably smaller projection to the ph. Both are entirely ipsilateral. The fibers destined for the ph travel with the NOT-NRTP bundle, pass through the NRTP, traverse the medial longitudinal fasciculus, and are distributed to the rostral one-half of the ph. The retrograde HRP studies confirm these pathways. The pretectal projections to the NRTP arise from neurons in the rostromedial NOT; those to the ph are located primarily in the rostral NOT although small numbers are found within the anterior, posterior, and olivary pretectal nuclei. Of major importance is the fact that the ph injections retrogradely label neurons within the NRTP and the adjacent paramedian pontine reticular formation. This NRTP-ph projection is entirely bilateral and arises from parts of both subdivisions of the nucleus targeted by NOT afferents.

Both the direct NOT-ph and indirect NOT-NRTP-ph connections provide the anatomical basis for the relay of visual (optokinetic) information to the perihypoglossal complex and, presumably, by virtue of reciprocal ph-vestibular nuclear connections, to the vestibular nuclei itself. Such pathways confirm previous physiological studies in rat and, in particular, clarify the contrasting effects of electrolytic lesions of NRTP in rat which completely abolishes optokinetic nystagmus (OKN) (Cazin et al., 1980a) vs kainic acid lesions which produce only minor effects on OKN slow velocity (Hess et al., 1988). Given these differential effects, one concludes that the critical pathway for OKN passes in relation to, but is not significantly relayed by, the neurons of the NRTP or adjacent pontine tegmentum. The present studies suggest that one such fiber system is the NOT-ph bundle. How this relatively small projection compares to other possible fiber of passage systems remains to be determined electrophysiologically.

Keywords

Horizontal optokinetic nystagmus3H-leucinNucleus of the optic tractNucleus reticularis tegmenti pontisPrepositus hypoglossi nucleus
Type
Research Article
Information
Visual Neuroscience , Volume 2 , Issue 3 , March 1989 , pp. 275 - 286
Copyright
Copyright © Cambridge University Press 1989

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

Abols, L.A. & Basbaum, A.I. (1979). The posterior pretectal nucleus: evidence for a direct projection to the inferior olive of the cat. Neuroscience Letters 13, 111–116.CrossRefGoogle Scholar
Alley, K., Baker, R. & Simpson, J.I. (1975). Afferents to the vestibulo-cerebellum and the origin of the visual-climbing fibers in the rabbit. Brain Research 98, 582–589.CrossRefGoogle Scholar
Baker, R., Gresty, M. & Berthoz, A. (1975). Neuronal activity in the prepositus hypoglossi nucleus correlated with vertical and horizontal eye movement in the cat. Brain Research 101, 366–371.CrossRefGoogle Scholar
Balaban, C.D. (1983). A projection from the nucleus reticularis teg-menti pontis of Bechterew to the medial vestibular nucleus in rabbits. Experimental Brain Research 51, 304–309.CrossRefGoogle Scholar
Belknap, D.B. & McCrea, R.A. (1988). Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey. Journal of Comparative Neurology 268, 13–28.CrossRefGoogle ScholarPubMed
Benevento, L.A., Rezak, M. & Santos-Anderson, R. (1977). An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macaca mulatto): evidence for sensorimotor links to the thalamus and oculomotor nuclei. Brain Research 127, 197–218.CrossRefGoogle Scholar
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retinorecipient and nonretinorecipient 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
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.CrossRefGoogle ScholarPubMed
Blanks, R.H.I. & Precht, W. (1983). Responses of units in the rat cerebellar flocculus during optokinetic and vestibular stimulation. Experimental Brain Research 53, 1–15.CrossRefGoogle ScholarPubMed
Blanks, R.H.I. & Torigoe, Y. (1982). Midbrain afferents to nucleus reticularis tegmenti ponti (NRTP). Investigative Opthalmology and Visual Science 22, 86.Google Scholar
Blanks, R.H.I., Volkind, R., Precht, W. & Baker, R. (1977). Responses of cat prepositus hypoglossi neurons to horizontal angular acceleration. Neuroscience 2, 391–403.CrossRefGoogle ScholarPubMed
Brodal, A. (1952). Experimental Demonstration of cerebellar connections from the perihypoglossal nuclei (nucleus intercalatus, nucleus prepositus hypoglossi, and nucleus of Roller) in the cat. Journal of Anatomy 86, 110–128.Google Scholar
Burne, R.A., Azizi, S.A., Mihatloff, G.A. & Woodward, D.J. (1981). The tectopontine projection in the rat with comments of visual pathways to the basilar pons. Journal of Comparative Neurology 202, 287–307.CrossRefGoogle Scholar
BÜttner-Ennever, J.A. & Henn, V. (1976). An autoradiographic study of the pathway from the pontine reticular formation involved in horizontal eye movements. Brain Research 108, 155–164.CrossRefGoogle ScholarPubMed
Carpenter, M.B. & Plerson, R.J. (1973). Pretectal region and the pupillary light reflex. An anatomical analysis in the monkey. Journal of Comparative Neurology 149, 271–300.CrossRefGoogle ScholarPubMed
Cazin, L., Precht, W. & Lannou, J. (1980 a). Pathways mediating optokinetic responses of vestibular nucleus neurons in the rat. Pflügers Archive 348, 19–29.CrossRefGoogle Scholar
Cazin, L., Precht, W. & Lannou, J. (1980 b). Firing characteristics of neurons mediating optokinetic responses to rat's vestibular neurons. Pflügers Archive 386, 221–230.CrossRefGoogle ScholarPubMed
Cazin, L., Magnin, M. & Lannou, J. (1982 a). Noncerebellar afferents to the vestibular nuclei involving the prepositus hypoglossi complex: an autoradiographic study in the rat. Experimental Brain Research 48, 309–313.CrossRefGoogle Scholar
Cazin, L., Precht, W. & Lannou, J. (1982 b). An electrophysiolog-ical study of the pathways from the retina to the vestibular nuclei in the rat. Neuroscience Letters (Suppl.) 10, 108.Google Scholar
Cazin, L., Lannou, J. & Precht, W. (1984). An electrophysiological study of pathways mediating optokinetic responses to the vestibular nucleus in the rat. Experimental Brain Research 54, 337–348.CrossRefGoogle Scholar
Collewijn, H. (1975 a). Oculomotor areas in the rabbit's midbrain and pretectum. Journal of Neurobiology 6, 3–22.CrossRefGoogle ScholarPubMed
Collewijn, H. (1975 b). Direction-selective units in the rabbit's nucleus of the optic tract. Brain Research 100, 489–508.CrossRefGoogle ScholarPubMed
Cowan, W.M., Gottlieb, D.I., Hendrickson, A.E., Price, J.L. & Woolsey, T.A. (1972). The autoradiographic demonstration of axonal connections in the central nervous system. Brain Research 37, 21–51.CrossRefGoogle ScholarPubMed
Crandall, W.F. & Keller, E.L. (1985). Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. Journal of Neurophysiology 54, 1326–1345.CrossRefGoogle ScholarPubMed
de Olmos, J., Hardy, H. & Heimer, L. (1978). The afferent connections of the main and the accessory olfactory bulb formations in the rat: an experimental HRP study. Journal of Comparative Neurology 181, 213–244.CrossRefGoogle ScholarPubMed
FifkÖváa, E. & Maršala, J. (1967). Stereotaxic atlas for the cat, rabbit, and rat. In Electrophysiological Methods in Biological Research, ed. BureŠ, J., Petráň, M. & Zachar, J., pp. 653–711. New York: Academic Press.CrossRefGoogle Scholar
Gerrits, N.M., Epema, A.H. & Voogd, J. (1984). The mossy fiber projection of the nucleus reticularis tegmenti pontis to the flocculus and adjacent ventral paraflocculus in the cat. Neuroscience 11, 627–644.CrossRefGoogle Scholar
Gerrits, N.M. & Voogd, J. (1986). The nucleus reticularis tegmenti pontis and adjacent rostral paramedian reticular formation; differential projections to the cerebellum and the caudal brain stem. Experimental Brain Research 62, 29–45.CrossRefGoogle Scholar
Giolli, R.A., Blanks, R.H.I. & Torigoe, Y. (1984). The efferent projections of the medial terminal nucleus of the accessory optic system of the rabbit and rat as studied using anterograde and retrograde neuronal transport methods. Journal of Comparative Neurology 227, 228–251.CrossRefGoogle Scholar
Graybiel, A.M. (1974 a). Some efferents of the pretectal region in the cat. Anatomical Records 178, 365.Google Scholar
Graybiel, A.M. (1974 b). Visuo-cerebellar and cerebello-visual connections involving the ventral lateral geniculate nucleus. Experimental Brain Research 20, 303–306.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1977). Direct and indirect preoculomotor pathways of the brain stem: an autoradiographic study of the pontine reticular formation in the cat. Journal of Comparative Neurology 175, 37–78.CrossRefGoogle ScholarPubMed
Gregory, K. (1985). The dendritic architecture of the visual pretectal nuclei of the rat: a study with the Golgi-Cox method. Journal of Comparative Neurology 234, 122–135.CrossRefGoogle Scholar
Harting, J.K., Hashjkawa, T. & Van Leshout, D. (1986). Laminar distribution of tectal, parabigeminal, and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus. Brain Research 366, 358–363.CrossRefGoogle Scholar
Hess, B.J.M., Blanks, R.H.I., Lannou, J. & Precht, W. (1986). Lesion of the nucleus reticularis tegmenti pontis (NRTP) prevents the charge of the velocity storage in the rat. Neuroscience Letters (Suppl.) 26, 327.Google Scholar
Hess, B.J.M., Blanks, R.H.I., Lannou, J. & Precht, W. (1988). Effects of kainic acid lesions of the nucleus reticularis tegmenti pontis on fast and slow phases of vestibulo-ocular and optokinetic reflexes in the pigmented rat. Experimental Brain Research (Submitted).Google Scholar
Hoffmann, K.P. & Schopmann, A. (1975). Retinal Input To Direction Selective cells in the nucleus tractus opticus of the cat. Brain Research 99, 359–366.CrossRefGoogle ScholarPubMed
Holstege, G. & Collewun, H. (1982). The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. Journal of Comparative Neurology 209, 139–175.CrossRefGoogle ScholarPubMed
Ito, M. (1984). The Cerebellum and Neural Control. New York: Raven Press.Google Scholar
Itoh, K. (1977). Efferent projections of the pretectum in the cat. Experimental Brain Research 30, 89–105.CrossRefGoogle ScholarPubMed
Keller, E.L. & Crandall, W.F. (1981). Neural activity in the nucleus reticularis tegmenti pontis in the monkey related to eye movements and visual stimulation. Annals of New York Academy of Sciences 374, 249–261.CrossRefGoogle ScholarPubMed
Keller, E.L. & Crandall, W.F. (1983). Neuronal responses to opto-kinetic stimuli in the pontine nuclei of behaving monkey. Journal of Neurophysiology 49, 169–187.CrossRefGoogle Scholar
Korp, B., Blanks, R.H.I. & Torigoe, Y. (1985). Pathways mediating horizontal optokinetic nystagmus, nucleus of the optic tract projections to the nucleus reticularis tegmenti pontis, and prepositus hypoglossi. Society of Neuroscience Abstracts 11, 25.1.Google Scholar
Kotchabhakdi, N., Hoddevrx, G.H. & Walberg, F. (1978). Cerebellar afferent projections from the perihypoglossal nuclei: an experimental study with the method of retrograde axonal transport of horseradish peroxidase. Experimental Brain Research 31, 13–29.Google ScholarPubMed
Langer, T., Fuchs, A.F., Scudder, C.A. & Chubb, M.C. (1985). Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 235, 1–25.CrossRefGoogle Scholar
Lopez-Barneo, J., Darlot, C. & Berthoz, A. (1979). Functional role of the prepositus hypoglossi nucleus in the control of gaze. Progress in Brain Research 50, 667–679.CrossRefGoogle ScholarPubMed
Mackay-Sim, A., Sefton, A.J. & Martin, P.R. (1983). Subcortical projections to lateral geniculate and thalamic reticular nuclei in the hooded rat. Journal of Comparative Neurology 213, 24–35.CrossRefGoogle ScholarPubMed
Maekawa, K. & Kimura, M. (1981). Electrophysiological study of the nucleus of the optic tract that transfers signals to the nucleus reticularis tegmenti pontis —the visual mossy fiber pathway to the cerebellar flocculus. Brain Research 221, 456–462.CrossRefGoogle Scholar
Maekawa, K. & Simpson, J.I. (1972). Climbing fiber activation of Purkinje cells in the flocculus by impulses transferred through the visual pathway. Brain Research 39, 245–251.CrossRefGoogle ScholarPubMed
Maekawa, K. & Takeda, T. (1975). Mossy fiber responses evoked in the cerebellar flocculus in rabbits by stimulation of the optic pathway. Brain Research 98, 590–595.CrossRefGoogle Scholar
Maekawa, K., Kimura, M. & Takeda, T. (1981 a). Mossy fiber activation of the cerebellar flocculus from the visual system. Annals of New York Academy of Sciences 374, 476–490.CrossRefGoogle ScholarPubMed
Maekawa, K., Takeda, T. & Kimura, M. (1981 b). Neural activity of nucleus reticularis tegmenti pontis. The origin of visual mossy fiber afferents to the cerebellar flocculus of rabbits. Brain Research 210, 17–30.CrossRefGoogle Scholar
Maekawa, K., Takeda, T. & Kimura, M. (1984). Responses of the nucleus of the optic tract neurons projecting to the nucleus reticularis tegmenti pontis upon optokinetic stimulation in the rabbit. Neuroscience Research 2, 1–25.CrossRefGoogle Scholar
Magnin, M., Courjon, J.H. & Flandrin, J.M. (1983). Possible visual pathways to the cat vestibular nuclei involving the nucleus prepositus hypoglossi. Experimental Brain Research 51, 298–303.CrossRefGoogle Scholar
McCrea, R.A. & Baker, R. (1985). Anatomical connections of the nucleus prepositus of the cat. Journal of Comparative Neurology 237, 377–407.CrossRefGoogle ScholarPubMed
McCrea, R.A., Baker, R. & Delgado-Garcia, J. (1979). Afferent and efferent organization of the prepositus hypoglossi nucleus. Progress in Brain Research 50, 653–665.CrossRefGoogle ScholarPubMed
Mihailoff, G.A., McArdle, C.B. & Adams, C.E. (1981). The cyto-architecture, cytology, and synaptic organization of the basilar pontine nuclei in the rat. I. Nissl and Golgi studies. Journal of Comparative Neurology 195, 181–201.CrossRefGoogle Scholar
Miyashita, Y., Ito, M., Jastreboff, P.J., Maekawa, K. & Nagao, S. (1980). Effect upon eye movements of rabbits induced by severance of mossy fiber visual pathway to cerebellar flocculus. Brain Research 198, 210–215.CrossRefGoogle ScholarPubMed
Mizuno, N., Mochizuki, K., Akimoto, C. & Matsushtma, R. (1973). Pretectal projections to the inferior olive in the rabbit. Experimental Neurology 39, 498–506.CrossRefGoogle Scholar
Mizuno, N., Nakamura, Y. & Iwahori, N. (1974). An electron microscope study of the dorsal cap of the inferior olive in the rabbit, with special reference to the pretecto-olivary fibers. Brain Research 77, 385–395.CrossRefGoogle Scholar
Nakao, S., Curthoys, I.S. & Markham, C.H. (1980). Eye-movement-related neurons in the cat pontine reticular formation: projection to the flocculus. Brain Research 183, 291–299.CrossRefGoogle Scholar
Pompeiano, O., Mergner, T. & Corvaja, N. (1978). Commissural perihypoglossal and reticular afferent projections to the vestibular nuclei in the cat. An experimental anatomical study with the method of the retrograde transport of horseradish peroxidase. Archives Italaliennes de Biologie 116, 130–172.Google Scholar
Precht, W., Blanks, R.H.I., Strata, P. & Montarolo, P. (1985). On the role of the subprimate cerebellar flocculus in the optokinetic reflex and visual-vestibular interaction. In Cerebellar Functions, ed. Bloedel, J.R., Dichgans, W. & Precht, W., pp. 86–108. Heidelberg: Springer Verlag.Google Scholar
Precht, W., Caztn, L., Blanks, R.H.I. & Lannou, J. (1982). Anatomy and physiology of the optokinetic pathways to the vestibular nuclei in the rat. In Physiological and Pathological Aspects of Eye Movements, ed. Roucoux, A. & Crommelinck, M., pp. 153–172. The Hague: W. Junk Publishers.CrossRefGoogle Scholar
Precht, W. & Strata, P. (1980). On the pathway mediating optokinetic responses in vestibular nuclear neurons. Neuroscience 5, 777–787.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1981). The Use of Control Systems Analysis in the neurophysiology of eye movements. Annual Reviews of Neuroscience (Review) 4, 463–503.CrossRefGoogle ScholarPubMed
Sato, Y., Kawasaki, T. & Ikarashi, K. (1983). Afferent projections from the brainstem to the three floccular zones in cats. II. Mossy fiber projections. Brain Research 111, 37–48.CrossRefGoogle Scholar
Simpson, J.I. & Soodak, R.E. (1978). The accessory optic system. A visual system in vestibular coordinates. Neuroscience (Abstract) 4, 645.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. In Neuroanatomy of the Oculomotor System, ed. BÜttner-Ennever, J.North Holland, Amsterdam: Elsevier (in press).Google Scholar
Taber, E., Brodal, A. & Walberg, F. (1960). The raphe nuclei of the brainstem in the cat. I. Normal topography and cytoarchitecture and general discussion. Journal of Comparative Neurology 114, 161–188.CrossRefGoogle ScholarPubMed
Terasawa, K., Otani, K. & Yamada, J. (1979). Descending pathways of the nucleus of the optic tract in the rat. Brain Research 173, 405–417.CrossRefGoogle ScholarPubMed
Torigoe, Y., Blanks, R.H.I. & Precht, W. (1986 a). Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. I. Cytoarchitecture, topography, and cerebral cortical afferents. Journal of Comparative Neurology 243, 71–87.CrossRefGoogle Scholar
Torigoe, Y., Blanks, R.H.I. & Precht, W. (1986 b). Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. II. Subcortical afferents demonstrated by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 243, 88–105.CrossRefGoogle ScholarPubMed
Torigoe, Y., Blanks, R.H.I. & Precht, W. (1988). Anatomical studies on the nucleus reticularis tegmenti pontis in the pigmented rat. III. Efferent projections demonstrated by anterograde 3H-leucine autoradiography and retrograde transport of horseradish peroxi dase. In preparation.Google Scholar
Waespe, W., Cohen, B. & Raphan, T. (1983). Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interaction: effects of lesions. Experimental Brain Research 50, 9–33.CrossRefGoogle ScholarPubMed
Waespe, W. & Henn, V. (1981). Visual-vestibular interaction in the alert monkey. I. Input activity. Experimental Brain Research 43, 337–348.CrossRefGoogle ScholarPubMed
Walberg, F., Nordby, T., Hoffmann, K.P. & Hollander, H. (1981). Olivary afferents from the pretectal nuclei in the cat. Anatomy and Embryology 161, 291–304.CrossRefGoogle ScholarPubMed
Weber, J.T. & Harting, J.K. (1980). The efferent projections of the pretectal complex. An autoradiographic and horseradish peroxidase analysis. Brain Research 194, 1–28.CrossRefGoogle ScholarPubMed
Weber, J.T., Chen, I-Li & Hutchins, B. (1986). The pretectal complex of the cat: cells of origin of projections to the pulvinar nucleus. Brain Research 397, 389–394.CrossRefGoogle Scholar
Yamamoto, M. (1979). Topographical Representation in rabbit cerebellar flocculus for various afferent inputs from the brain stem inves-tigated by means of retrograde axonal transport of horseradish peroxidase. Neuroscience Letters 12, 29–34.CrossRefGoogle Scholar