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The pupillary light reflex in normal and innate microstrabismic cats, II: Retinal and cortical input to the nucleus praetectalis olivaris

Published online by Cambridge University Press:  02 June 2009

C. Distler  and
K.-P. Hoffmann
C. Distler
Affiliation:
Lehrstuhl fuer Allgemeine Zoologie und Neurobiologie, Ruhr-Universitaet Bochum, Bochum, FRG
K.-P. Hoffmann
Affiliation:
Lehrstuhl fuer Allgemeine Zoologie und Neurobiologie, Ruhr-Universitaet Bochum, Bochum, FRG
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Abstract

The anatomical substrate of the pupillary light reflex was investigated in normal and innate microstrabismic cats using anatomical methods as well as electrical stimulation. The bilateral retinal input to the nucleus praetectalis olivaris (NPO), the pretectal relay station in the subcortical pupilloconstrictor pathway, was identified to come from the ventral retina where the upper visual field is represented. Orthodromic electrical stimulation revealed that retinal information is transmitted to on-tonic neurons in the NPO mainly via slowly conducting axons probably originating from W- and X-type retinal ganglion cells.

For the first time, a direct cortical input to on-tonic neurons in the NPO could be demonstrated. This cortical input originates from caudolateral parts of the occipital cortex. Putative input structures are those subdivisions of areas 19 and 20a where the upper part of the visual field is represented.

A direct, predominantly contralateral projection with a weak ipsilateral component from NPO to the nucleus of Edinger-Westphal, and an interhemispheric connection between the NPOs could be demonstrated. With respect to the anatomical connections as described in this study, no differences between normal and innate microstrabismic cats could be found.

The results are discussed with respect to the binocular summation of the pupillary light reflex and its reduction in subjects with impaired binocular vision.

Keywords

Pupilloconstrictor pathwayNucleus praetectalis olivarisArea 20aRetinaCatStrabismus
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 139 - 153
Copyright
Copyright © Cambridge University Press 1989

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References

Ballas, I. & Hoffmann, K.-P. (1985). A correlation between receptive-field properties and morphological structures in the pretectum of the cat. Journal of Comparative Neurology 238, 417–428.CrossRefGoogle ScholarPubMed
Ballas, I. & Hoffmann, K.-P. (1990). Retinal input to the pretectum in the cat (in preparation).Google Scholar
Ballas, I., Hoffmann, K.-P. & Wagner, H.J. (1981). Retinal projection to the nucleus of the optic tract in the cat as revealed by retrograde transport of horseradish peroxidase. Neuroscience Letters 26, 197–202.CrossRefGoogle Scholar
Bando, T. (1985). Pupillary constriction evoked from the posterior medial lateral suprasylvian (PMLS) area in cats. Neuroscience Research 2, 472–485.CrossRefGoogle ScholarPubMed
Bando, T. (1987). Depressant effect of cooling of the postero-lateral occipital cortex on pupillo-constriction responses evoked from the lateral suprasylvian area in cats. Neuroscience Research 4, 316–322.CrossRefGoogle ScholarPubMed
Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. & Tsukahara, N. (1981). Cortical neurons in and around the Clare-Bishop area related with lens accommodation in the cat. Brain Research 225, 195–199.CrossRefGoogle ScholarPubMed
Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. & Tsukahara, N. (1984). Physiological identification of midbrain neurons related to lens accommodation in cats. Journal of Neurophysiology 52, 870–878.CrossRefGoogle ScholarPubMed
Barbur, J.L. & Forsyth, P.M. (1986). Can the pupil response by used as a measure of the visual input associated with the geniculo-striate pathway? Clinical and Vision Sciences 1, 107–111.Google Scholar
Barris, R.W. (1936). A pupilloconstrictor area in the cerebral cortex of the cat and its relationship to the pretectal area. Journal of Comparative Neurology 63, 353–368.CrossRefGoogle Scholar
Bechterew, W. (1883). Über den Verlauf der die pupille verengenden nervenfasern im gehirn und über die lokalisation eines centrums für die iris und contraction der augenmuskeln. Pflügers Archive 31, 68–87.CrossRefGoogle Scholar
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
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.CrossRefGoogle ScholarPubMed
Breen, L.A., Burde, R.M. & Loewy, A.D. (1983). Brainstem connections to the Edinger-Westphal nucleus of the cat: a retrograde tracer study. Brain Research 261, 303–306.CrossRefGoogle Scholar
Campbell, G. & Lieberman, A.R. (1985). The olivary pretectal nucleus: experimental anatomical studies in the rat. Philosophical Transactions of the Royal Society B (London) 310, 573–609.Google ScholarPubMed
Capenter, M.B. & Pierson, R.J. (1973). Pretectal region and the pupillary light reflex. An anatomical analysis in the monkey. Journal of Comparative Neurology 149, 271–300.CrossRefGoogle Scholar
Cavada, C. & Reinoso-Suarez, F. (1983). Afferent connections of area 20 in the cat studied by means of the retrograde axonal transport of horseradish peroxidase. Brain Research 270, 319–324.CrossRefGoogle ScholarPubMed
Cleland, G.B. & Levick, W.R. (1974). Properties of rarely encountered types of ganglion cells in the cat's retina and an overall classification. Journal of Physiology 240, 457–492.CrossRefGoogle Scholar
Cleland, G.B., Dubin, M.W. & Lewick, W.R. (1971). Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. Journal of Physiology (London) 217, 473–496.CrossRefGoogle ScholarPubMed
Dineen, J.T. & Hendrickson, A. (1983). Overlap of retinal and pre-striate cortical pathways in the primate pretectum. Brain Research 278, 250–254.CrossRefGoogle Scholar
Distler, C. & Hoffmann, K.-P. (1989). The pupillary light reflex in normal and innate microstrabismic cats, I: Behavior and receptive-field analysis in the nucleus praetectalis olivaris. Visual Neuroscience 3, 127–138.CrossRefGoogle ScholarPubMed
Dreher, B., Leventhal, A.G. & Hale, P.T. (1980). Geniculate input to cat visual cortex: a comparison of area 19 with areas 17 and 18. Journal of Neurophysiology 44, 804–826.CrossRefGoogle Scholar
Fuse, G. (1936). Ueber einen bisher unbekannten, den Nucl. olivaris corporis quadrigemini anterioris, beim Menschen und Tier. Arbeiten aus dem anatomischen Institut der Universitaet Sendai 19, 49–486.Google Scholar
Gamlin, P.D.R., Reiner, A., Erichsen, J.T., Karten, H.J. & Cohen, D.H. (1984). The neuronal substrate for the pupillary light reflex in the pigeon (Columba livia). Journal of Comparative Neurology 226, 523–543.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R. & Cohen, D.H. (1988). Projections of the retinorecipient pretectal nuclei in the pigeon (Columba livia). Journal of Comparative Neurology 269, 18–46.CrossRefGoogle ScholarPubMed
Giolli, R.A., Towns, L.C. & Haste, D.A. (1974). The mode of inner-vation of portions of the anterior and posterior pretectal nuclei of the rabbit by axons arising from the visual cortex. Journal of Comparative Neurology 155, 177–194.CrossRefGoogle Scholar
Graybiel, A.M. (1974). Some efferents of the pretectal region in the cat. Anatomical Records 178, 365.Google Scholar
Hada, J., Yamagata, Y. & Hayashi, Y. (1985). Identification of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus in the cat. Brain Research 358, 398–403.CrossRefGoogle Scholar
Hada, J., Yamagata, Y. & Hayashi, Y. (1986). Visual response properties of ventral lateral geniculate nucleus cells projecting to the pretectum and superior colliculus in the cat. Brain Research 363, 165–169.CrossRefGoogle Scholar
Hoffmann, K.-P. (1970). Retinotopische beziehungen und struktur re-zeptiver felder im tectum opticum und praetectum der katze. Zeit-schrift für Vergleichende Physiologie 67, 26–57.CrossRefGoogle Scholar
Hoffmann, K.-P. (1973). Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive-field properties. Journal of Neurophysiology 36, 409–424.CrossRefGoogle Scholar
Hoffmann, K.-P. & Schoppmann, A. (1975). Retinal input to direction selective cells in the nucleus tractus opticus of the cat. Brain Research 99, 359–366.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Schoppmann, A. (1984). Shortage of binocular cells in area 17 of visual cortex in cats with congenital strabismus. Experimental Brain Research 55, 470–482.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. & Stone, J. (1985). Retinal input to the nucleus of the optic tract of the cat assessed by antidromic activation of ganglion cells. Experimental Brain Research 59, 395–403.CrossRefGoogle Scholar
Horn, A.K.E. & Hoffman, K.-P. (1987). Combined GABA-immuno-histochemistry and TMP-HRP histochemistry of pretectal nuclei projecting to the inferior olive in rats, cats, and monkeys. Brain Research 409, 133–138.CrossRefGoogle Scholar
Hultborn, H., Mori, K. & Tsukahara, N. (1973). The neuronal pathway subserving the pupillary light reflex and its facilitation from cerebellar nuclei. Brain Research 63, 357–361.CrossRefGoogle ScholarPubMed
Hultborn, H., Mori, K. & Tsukahara, N. (1978). The neuronal pathway subserving the pupillary light reflex. Brain Research 159, 255–267.CrossRefGoogle ScholarPubMed
Hutchins, B. & Weber, J.T. (1985). The pretectal olivary nucleus of the cat: evidence for a two-tailed structure. Brain Research 331, 150–154.CrossRefGoogle ScholarPubMed
Imai, H., Shoumura, K., Kuchiiwa, T. & Kuchiiwa, S. (1984). Pupillomotor areas in the rabbit visual cortex. Neuroscience Letters 48, 13–17.CrossRefGoogle ScholarPubMed
Inoue, T. & Kiribuchi, T. (1985). Cortical and subcortical pathways for pupillary reactions in rabbits. Japanese Journal of Ophthalmology 29, 63–70.Google ScholarPubMed
Itoh, K. (1977). Efferent projections of the pretectum in the cat. Experimental Brain Research 30, 89–105.CrossRefGoogle ScholarPubMed
Jampel, R.S. (1960). Convergence, divergence, pupillary reactions, and accomodation of the eyes from Faradic stimulation of the macaque brain. Journal of Comparative Neurology 115, 371–399.CrossRefGoogle Scholar
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–338.CrossRefGoogle ScholarPubMed
Kawamura, S., Sprague, J.M. & Niimi, K. (1974). Corticofugal projections from the visual cortices to the thalamus, pretectum, and superior colliculus in the cat. Journal of Comparative Neurology 158, 339–362.CrossRefGoogle Scholar
Koontz, M.A., Rodieck, R.W. & Farmer, S.G. (1985). The retinal projection to the cat pretectum. Journal of Comparative Neurology 236, 42–59.CrossRefGoogle Scholar
Kuchiiwa, S., Shoumura, K., Kuchiiwa, T. & Imai, H. (1984). Affer-ents to the cortical pupilloconstrictor areas of the cat traced with HRP. Experimental Brain Research 54, 377–381.CrossRefGoogle Scholar
Kuchiiwa, S., Kuchiiwa, T., Matsue, H. & Sukekawa, K. (1985). Efferent connections of area 20 in the cat: WGA-HRP and autoradiographic studies. Experimental Brain Research 60, 179–183.CrossRefGoogle ScholarPubMed
Laties, A.M. & Sprague, J.M. (1966). The projection of the optic fibers to the visual centers in the cat. Journal of Comparative Neurology 127, 35–70.CrossRefGoogle Scholar
Magoun, H.W. (1935). Maintenance of the light reflex after destruction of the superior colliculus in the cat. American Journal of Physiology 111, 91.CrossRefGoogle Scholar
Magoun, H.W., Atlas, D., Hare, W.K. & Ranson, S.W. (1936). The afferent path of the pupillary light reflex in the monkey. Brain 59, 234–249.CrossRefGoogle Scholar
Matsushita, T. (1959). The pupilloconstrictor and pupillodilator response area in the pretectal region, mesencephalic central grey matter, and its periphery in cats. Folia Psychologica et Neurologica Japonica 13, 262–300.Google Scholar
Mesulam, M.M. (1978). Tetramethyl benzidine for horseradish peroxidase histochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.CrossRefGoogle ScholarPubMed
Pierson, R.J. & Carpenter, M.B. (1974). Anatomical analysis of pupillary reflex pathways in Rhesus monkey. Journal of Comparative Neurology 158, 121–144.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Rosenquist, A.C. (1980). Connections of the par-vocellular C laminae of the dorsal lateral geniculate nucleus with the visual cortex in the cat. Brain Research 199, 447–451.CrossRefGoogle ScholarPubMed
Ranson, S.W. & Magoun, H.W. (1933). The central path of the pupilloconstrictor reflex in response to light. Archive of Neurology and Psychiatry 30, 1193–1204.CrossRefGoogle Scholar
Reiner, A., Karten, H.J., Gamlin, P.D.R. & Erichsen, J.T. (1983). Parasympathetic ocular control. Functional subdivisions and circuitry of the avian nucleus of Edinger-Westphal. Trends in Neuroscience 6, 140–145.CrossRefGoogle Scholar
Sawai, H., Fukuda, Y. & Wakakuwa, K. (1985). Axonal projections of X cells to the superior colliculus and to the nucleus of the optic tract in cats. Brain Research 341, 1–6.CrossRefGoogle Scholar
Schoppmann, A. & Hoffmann, K.-P. (1979). A comparison of visual responses in two pretectal nuclei and in the superior colliculus of the cat. Experimental Brain Research 35, 495–510.CrossRefGoogle ScholarPubMed
Schoppmann, A. & Hoffmann, K.-P. (1985). The development of eye alignment in normal and naturally microstrabismic kittens. Investigative Ophthalmology and Visual Sciences 26, 350–358.Google ScholarPubMed
Shoumura, K. & Imai, H. (1986). Pupillary response evoked by electrical stimulation of area praetectalis in cats. Japanese Journal of Ophthalmology 30, 436–452.Google Scholar
Shoumura, K., Kuchhwa, S. & Sukekawa, K. (1982). Two pupilloconstrictor areas in the occipital cortex of the cat. Brain Research 247, 134–137.CrossRefGoogle ScholarPubMed
Shoumura, K., Kuchiiwa, S., Imai, H., Kuchiiwa, T. & Kumakura, T. (1984). Cerebral cortical control of pupillary movements: anatomical and physiological studies in the cat. Asian Medicine Journal 27, 16–33.Google Scholar
Shoumura, K., Imai, H., Kimura, S., Suzuki, T. & Ara, M. (1987). Posterior commissural connections of area pretectalis and neighbouring structures in cat, with special reference to pupilloconstructory pathway via posterior commissure. Japanese J. of Ophthalmology 31, 289–304.Google ScholarPubMed
Sireteanu, R. (1987). Binocular luminance summation in humans with defective binocular vision. Investigative Ophthalmology and Visual Sciences 28, 349–355.Google ScholarPubMed
Sireteanu, R. & Altmann, L. (1987). Binocular luminance summation in young kittens and adult strabismic cats. Investigative Ophthalmology and Visual Sciences 28, 343–348.Google ScholarPubMed
Slooter, J. & Van Norren, D. (1980). Visual acuity measured with pupil response to checkerboard stimuli. Investigative Ophthalmology and Visual Sciences 19, 105–108.Google ScholarPubMed
Spear, P.D., Smith, D.C. & Williams, L.L. (1977). Visual receptive-field properties of single neurons in cat's ventral lateral geniculate nucleus. Journal of Neurophysiology 40, 390–409.CrossRefGoogle ScholarPubMed
Stanford, L.R. (1987). W cells in the cat retina: correlated morphological and physiological evidence for two distinct classes. Journal of Neurophysiology 57, 218–244.CrossRefGoogle ScholarPubMed
Steiger, H.J. & Büttner-Ennever, J.A. (1979). Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase. Brain Research 160, 1–15.CrossRefGoogle ScholarPubMed
Stone, J. & Hoffmann, K.-P. (1972). Very slow-conducting ganglion cells in the cat's retina: a major, new functional type? Brain Research 43, 610–616.CrossRefGoogle Scholar
Stone, J. & Fukuda, Y. (1974). Properties of cat retinal ganglion cells: a comparison of W cells with X and Y cells. Journal of Neurophysiology 37, 722–748.CrossRefGoogle ScholarPubMed
Trejo, L.J. & Cicerone, C.M. (1984). Cells in the pretectal olivary nucleus are in the pathway for the direct light reflex of the pupil in the rat. Brain Research 300, 49–62.CrossRefGoogle ScholarPubMed
Tusa, R.J., Palmer, L.A. & Rosenquist, A.C. (1978). The retinotopic organization of area 17 (striate cortex) in the cat. Journal of Comparative Neurology 177, 213–236.CrossRefGoogle ScholarPubMed
Tusa, R.J., Rosenquist, A.C. & Palmer, L.A. (1979). Retinotopic organization of areas 18 and 19 in the cat. Journal of Comparative Neurology 185, 657–678.CrossRefGoogle Scholar
Tusa, R. J. & Palmer, L.A. (1980). Retinotopic organization of areas 20 and 21 in the cat. Journal of Comparative Neurology 193, 147–164.CrossRefGoogle ScholarPubMed
Updyke, B.V. (1977). Topographic organization of the projections from cortical areas 17, 18, and 19 onto the thalamus, pretectum, and superior colliculus in the cat. Journal of Comparative Neurology 173, 81–122.CrossRefGoogle Scholar
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
Yoshoka, H. (1957). The pupilloconstrictor and pupillodilator response area in rabbit's pretectal region, in the central grey matter of mid-brain, and its periphery. Folia Psychologica et Neurologica Japonica 11, 70–100.Google Scholar