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The perihypoglossal projection to the superior colliculus in the rhesus monkey

Published online by Cambridge University Press:  02 June 2009

Rosi Hartwich-Young ,
Jon S. Nelson  and
David L. Sparks
Rosi Hartwich-Young
Affiliation:
Alcon Laboratories, Inc., Fort Worth
Jon S. Nelson
Affiliation:
Department of Physical Therapy, College of St. Scholastica, Duluth
David L. Sparks
Affiliation:
Department of Psychology, University of Pennsylvania, Philadelphia
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Abstract

The projection of the perihypoglossal (PH) complex to the superior colliculus (SC) in the rhesus monkey was investigated using the retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase (WGA-HRP). Following physiological identification by electrical stimulation and multiunit recording, small injections of the tracer were placed within the SC of three monkeys. The largest numbers of retrogradely labeled neurons within the PH complex were found in the contralateral nucleus prepositus hypoglossi (NPH), in the laterally adjacent medial vestibular nucleus, and in the ventrally adjacent reticular formation (the nucleus reticularis supragigantocellularis). These labeled neurons are strikingly heterogeneous in size and morphology. The nuclei supragenualis and intercalatus also contain numerous labeled neurons in the 2 cases in which the injections involve the caudal SC. Large numbers of retrogradely labeled neurons as well as anterogradely transported WGA-HRP are observed alo throughout the pontine and medullary reticular formation, including the midline raphe. The PH complex, particularly the NPH, is known to be involved in the coding of eye position and has been hypothesized to be a critical component of the “neural integrator.” Our data demonstrate the existence of a robust projection from the PH complex to the contralateral SC in the rhesus monkey. This projection may serve as the anatomical substrate by which a corollary of eye position could reach the SC. Such a signal is a prerequisite for the computation, at the collicular level, of saccadic motor error signals observed in the SC of rhesus monkeys.

Keywords

Nucleus prepositus hypoglossiSuperior colliculusWheat germ agglutinin-horseradish peroxidaseSaccadic motor errorEye position signalNeural integrator
Type
Research Articles
Information
Visual Neuroscience , Volume 4 , Issue 1 , January 1990 , pp. 29 - 42
Copyright
Copyright © Cambridge University Press 1990

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References

Anastasio, T.J. & Robinson, D.A. (1988). A single unit and lesion study of the primate nucleus prepositus hypoglossi (NPH). Investigative Ophthalmology and Visual Science 29, 167.Google Scholar
Belknap, C.B. & McCrea, R.A. (1988). Anatomical connection of the prepositus and abducens nuclei in the squirrel monkey. Journal of Comparative Neurology 268, 13–28.CrossRefGoogle ScholarPubMed
Brodal, A. (1983). The perihypoglossal nuclei in the macaque monkey and the chimpanzee. Journal of Comparative Neurology 218, 257–269.CrossRefGoogle ScholarPubMed
Cannon, S.C. & Robinson, D.A. (1987). Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. Journal of Neurophysiology 57, 1383–1409.CrossRefGoogle ScholarPubMed
Cazin, L., Magnin, M. & Lannou, L. (1982). Non-cerebellar visual afferents to the vestibular nuclei involving the prepositus hypoglossal complex: an autoradiographic study in the rat. Experimental Brain Research 48, 309–313.CrossRefGoogle Scholar
Cheron, B. & Godaux, E. (1987). Disabling of the oculomotor neural integrator by kainic acid injections in the prepositus-vestibular complex of the cat. Journal of Physiology 394, 267–290.CrossRefGoogle ScholarPubMed
Delgado-Garcia, J.M., Vidal, P.P., Gomez, C. & Berthoz, A. (1989). A neurophysiological study of prepositus hypoglossi neurons projecting to oculomotor and preoculomotor nuclei in the alert cat. Neuroscience 29, 291–307.CrossRefGoogle ScholarPubMed
Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.CrossRefGoogle Scholar
Graybiel, A.M. (1977). Direct and indirect preoculomotor pathways of the brainstem: an autoradiographic study of the pontine reticular formation in the cat. Journal of Comparative Neurology 175, 37–38.CrossRefGoogle ScholarPubMed
Hartwich-Young, R., Nelson, J.S. & Sparks, D.L. (1988). Perihypoglossal projections to superior colliculus in rhesus monkeys. Investigative Ophthalmology and Visual Science 29, 166.Google Scholar
Jay, M.F. & Sparks, D.L. (1987) Sensorimotor integration in the primate superior colliculus, II: Coordinates of auditory signals. Journal of Neurophysiology 57, 35–55.CrossRefGoogle ScholarPubMed
Langer, T., Kaneko, C.R.S., Scudder, C.A. & Fuchs, A.F. (1986). Afferents to the abducens nucleus in the monkey and cat. Journal of Comparative Neurology 245, 379–400.CrossRefGoogle Scholar
Leichnetz, G.R. (1985). The frontal eye field projects to the nucleus prepositus hypoglossi in the monkey. Neuroscience Letters 54, 185–188.CrossRefGoogle Scholar
Lopez-Barneo, J., Darlot, C., Berthoz, A. & Baker, R. (1982). Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. Journal of Neurophysiology 47, 329–352.CrossRefGoogle ScholarPubMed
Malpeli, J.G. & Schiller, P.H. (1979). A method of reversible inactivation of small regions of brain tissue. Journal of Neuroscience Methods 1, 143–151.CrossRefGoogle ScholarPubMed
May, P.J. & Porter, J.D. (1988). The brainstem sources of afferents to the superior colliculus in a primate. Anatomical Record 20, 62A.Google Scholar
Mays, L.E. & Sparks, D.L. (1980). Dissociation of visual and saccade-related responses in superior colliculus neurons. Journal of Neurophysiology 43, 207–232.CrossRefGoogle ScholarPubMed
McCrea, R.A. & Baker, R. (1985). Anatomical connections of the nucleus prepositus of the cat. Journal of Comparative Neurology 237, 377–407.CrossRefGoogle ScholarPubMed
McFarland, J.L. & Fuchs, A.F. (1986). Medullary eye-position inputs to the abducens nucleus. Society for Neuroscience Abstracts 12, 460.Google Scholar
Mehler, W.R., Feferman, M.E. & Nauta, W.J.H. (1960). Ascending axon degeneration following anterolateral cordotomy. An experimental study in the monkey. Brain 83, 718–750.CrossRefGoogle ScholarPubMed
Mesulam, M.-M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–107.CrossRefGoogle ScholarPubMed
Mesulam, M.-M., Hegarty, E., Barbas, H., Carson, K.A., Gower, E.C., Knapp, A.G., Moss, M.B. & Mufson, E.J. (1980). Additional factors influencing sensitivity in the tetramethyl benzidine method for horseradish peroxidase neurohistochemistry. Journal of Histochemistry and Cytochemistry 28, 1255–1259.CrossRefGoogle ScholarPubMed
Peck, C.K. (1986). Eye-position signals in cat superior colliculus. Experimental Brain Research 61, 447–450.CrossRefGoogle ScholarPubMed
Roucoux, A., Crommelinck, M. & Guitton, D. (1980). Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Experimental Brain Research 39, 75–85.CrossRefGoogle ScholarPubMed
Sparks, D.L., Holland, R. & Guthrie, B.L. (1976). Size and distribution of movement fields in the monkey superior colliculus. Brain Research 113, 21–34.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988). Frontal eye field efferents in the macaque monkey, II: Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.CrossRefGoogle ScholarPubMed
Stechison, M.T., Saint-Cyr, J.A. & Spence, S.J. (1985). Projections from the nuclei prepositus hypoglossi and intercalatus to the superior colliculus in the cat: an anatomical study using WGA-HRP. Experimental Brain Research 59, 139–150.CrossRefGoogle Scholar
Yingcharoen, K. & Rinvik, E. (1982). Branched projections from the nucleus prepositus hypoglossi to the oculomotor nucleus and the cerebellum. A retrograde fluorescent double-labelling study in the cat. Brain Research 246, 133–136.CrossRefGoogle Scholar