Hostname: page-component-78c5997874-fbnjt Total loading time: 0 Render date: 2024-11-17T03:22:16.908Z Has data issue: false hasContentIssue false
  • English
  • Français

The pupillary light reflex in normal and innate microstrabismic cats, I: Behavior and receptive-field analysis in 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
Get access Rights & Permissions [Opens in a new window]

Abstract

Neurons in the nucleus praetectalis olivaris (NPO) were antidromically identified by electrical stimulation of the nucleus of Edinger-Westphal (EW), the location of preganglionic pupilloconstrictor motoneurons. Electrical stimulation within the NPO leads to bilateral pupil constriction. Single neurons recorded in the NPO respond tonically to light stimuli, and their discharge frequency increases linearly with logarithmic increase in light intensity. This characteristic identifies NPO neurons as luminance detectors. They have large receptive fields mostly lying in the upper and contralateral quadrant of the visual field.

Cats with impaired binocular vision show a significantly reduced binocular summation of the pupillary light reflex (BSP), i.e. the increase of pupil constriction during binocular illumination when compared to monocular illumination is less than in normal animals. The investigation of ocular dominance and subthreshold binocular interactions in the NPO of normal and innate microstrabismic cats revealed two possible mechanisms for BSP and its reduction in strabismic subjects. First, the percentage of neurons increasing their discharge rate by illuminating either eye is significantly reduced in the NPO of innate microstrabismic cats (6.6%) when compared to normal cats (22% of all neurons tested). Second, in most NPO neurons of normal cats the subthreshold influence of the ipsilateral eye leads to an increase in neuronal activity during binocular stimulation when compared to monocular stimulation of the contralateral eye (binocular summation). The subthreshold influence of the ipsilateral eye in most NPO neurons of microstrabismic cats, however, is inhibitory, i.e. the neuronal discharge rate during binocular stimulation is decreased when compared to monocular stimulation of the contralateral eye (binocular inhibition). However, there is no significant correlation between BSP and binocularity in the NPO in individual animals. This suggests that BSP may be additionally influenced by visual structures other than NPO.

Keywords

PupilNucleus praetectalis olivarisMicrostrabismusCatBinocular summation of the pupillary light reflex
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 127 - 138
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

Alexandridis, E. (1982). Die Pupille. Berlin, Heidelberg, New York: Springer.CrossRefGoogle Scholar
Alexandridis, E. & Dodt, E. (1967). Pupillenlichtreflexe und pupillenweite einer staebchenmonochromatin. Graefes Archive of Klinical and Experimental Ophthalmology 173, 153–161.CrossRefGoogle Scholar
Alpern, M. & Campbell, F.W. (1962). The spectral sensitivity of the consensual light reflex. Journal of Physiology 164, 478–507.CrossRefGoogle ScholarPubMed
Aulhorn, E. (1967). Die Abhängigkeit der Sehschärfe von der Pupillenweite. Berichte der Deutschen Ophthalmologischen Gesellschaft 68, 304–309.Google Scholar
Avendano, C. & Juretschke, M.A. (1980). The pretectal region of the cat: a structural and topographical study with stereotaxic coordinates. Journal of Comparative Neurology 193, 69–88.CrossRefGoogle 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). Ueber den verlauf der die pupille verengenden nervenfasern im gehirn und ueber die lokalisation eines centrums für die iris und die contraktion der augenmuskeln. Pfluegers Archiv 31, 68–87.CrossRefGoogle Scholar
Berman, N. (1977). Connections of the pretectum in the cat. Journal of Comparative Neurology 174, 227–254.CrossRefGoogle ScholarPubMed
Berman, N. & Murphy, E.H. (1982). The critical period for alteration in cortical binocularity resulting from divergent and convergent strabismus. Developmental Brain Research 2, 181–202.CrossRefGoogle Scholar
Birch, E.E. & Held, R. (1983). The development of binocular summation in human infants. Investigative Ophthalmology and Visual Sciences 24, 1103–1107.Google ScholarPubMed
Breen, L.A., Burde, R.M. & Loewy, A.D. (1983). Brainstem connections to the Edinger-Westphal nucleus in 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 Scholar
Carpenter, M.B. & Person, 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
Cavaggioni, A., Madarasz, J. & Zampollo, A. (1968). Photic reflex and pretectal region. Archives Italiennes Biologiques 106, 227–242.Google Scholar
Clarke, R.J. & Ikeda, H. (1985 a). Luminance and darkness detectors in the olivary and posterior pretectal nuclei and their relationship to the pupillary light reflex in the rat, I: Studies with steady luminance levels. Experimental Brain Research 57, 224–232.Google Scholar
Clarke, R.J. & Ikeda, H. (1985 b). Luminance detectors in the olivary pretectal nucleus and their relationship to the pupillary light reflex in the rat, II: Studies using sinusoidal light. Experimental Brain Research 59, 83–90.CrossRefGoogle Scholar
Cynader, M. & Hoffmann, K.-P. (1981). Strabismus disrupts binocular convergence in cat nucleus of the optic tract. Developmental Brain Research 1, 132–136.CrossRefGoogle Scholar
Dineen, J.T. & Hendrickson, A. (1983). Overlap of retinal and pre-striate cortical pathways in the primate pretectum. Brain Research 278, 250–254.Google Scholar
Distler, C. & Hoffmann, K.-P. (1989). The pupillary light reflex in normal and innate microstrabismic cats, II: Retinal and cortical input to the nucleus praetectalis olivaris. Visual Neuroscience 3, 139–154.CrossRefGoogle Scholar
Doesschate, J. Ten & Alpern, M. (1965). Response of the pupil to steady-state retinal illumination: contribution by cones. Science 149, 989–991.Google Scholar
Doesschate, J. Ten & Alpern, M. (1967). Effect of photoexcitation of the two retinas on pupil size. Journal of Neurophysiology 30, 562–576.Google Scholar
Feldon, S., Feldon, P. & Kruoer, L. (1970). Topography of the retinal projection upon the superior colliculus in the cat. Vision Research 10, 135–143.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R., Reiner, A., Erichsen, J.T., Karten, H.J. & Cohen, D.H. (1984). The neural substrate for the pupillary light reflex in the pigeon (Columba livia). Journal of Comparative Neurology 226, 523–543.Google Scholar
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.Google Scholar
Hoffmann, K.-P. (1970). Retinotopische beziehungen und struktur re-zeptiver felder im tectum opticum und praetectum der katze. Zeitschrift für Vergteichende Physiologie 67, 26–57.CrossRefGoogle Scholar
Hoffmann, K.-P. (1983). Effects of early monocular deprivation on visual input to cat nucleus of the optic tract. Experimental Brain Research 51, 236–246.CrossRefGoogle ScholarPubMed
Hoffmann, K.-P. (1987). The influence of visual experience on the ontogeny of the optokinetic reflex in mammals. In Imprinting and Cortical Plasticity, ed. Rauschecker, J. & Marler, P., pp. 267–286. New York: Wiley.Google Scholar
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.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1965). Binocular interaction in striate cortex of kittens reared with artificial squint. Journal of Neurophysiology 28, 1041–1059.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. Journal of Physiology (London) 206, 419–436.Google 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.Google Scholar
Hutchins, B. & Weber, J.T. (1985). The pretectal olivary nucleus of the cat: evidence for a two-tailed structure. Brain Research 331, 150–154.Google Scholar
Imai, H., Shoumura, K., Kuchiiwa, T. & Kuchiiwa, S. (1984). Pupil-lomotor areas in the rabbit visual cortex. Neuroscience Letters 48, 13–17.Google Scholar
Inoue, T. & Kiribuchi, T. (1985). Cortical and subcortical pathways for pupillary reactions in rabbits. Japanese Journal of Ophthalmology 29, 63–70.Google Scholar
Jampel, R.S. (1960). Convergence, divergence, pupillary reactions, and accommodation of the eyes from Faradic stimulation of the macaque brain. Journal of Comparative Neurology 115, 371–399.Google 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
Koontz, M.A., Rodieck, R.W. & Farmer, S.G. (1985). The retinal projection to the cat pretectum. Journal of Comparative Neurology 236, 42–59.Google Scholar
Kuhlenbeck, H. & Miller, R.N. (1942). The pretectal region of the rabbit's brain. Journal of Comparative Neurology 76, 323–365.Google Scholar
Kuhlenbeck, H. & Miller, R.N. (1949). The pretectal region of the human brain. Journal of Comparative Neurology 91, 369–408.CrossRefGoogle ScholarPubMed
Magoun, H.W. (1935). Maintenance of the light reflex after destruction of the superior colliculus in the cat. American Journal of Physiology 111, 91.Google 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
Magoun, R.W. & Ranson, S.W. (1935). The central path of the light reflex: a study of the effects of lesions. Archives of Ophthalmology 13, 791.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 of Psychiatry and Neurology of Japan 13, 262–300.Google Scholar
Pierson, R.J. & Carpenter, M.B. (1974). Anatomical analysis of pupillary reflex pathways in the rhesus monkey. Journal of Comparative Neurology 158, 121–144.CrossRefGoogle ScholarPubMed
Ranson, S.W. & Magoun, H.W. (1933). The central path of the pupilloconstrictor reflex in response to light. Archives of Neurology and Psychiatry 30, 1193–1204.Google 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 Neuro-sciences 6, 140–145.Google Scholar
Romano, P. & Michels, M. (1985). Binocular luminance summation in infants. A test for stereopsis? Archives of Ophthalmology 103, 1840–1841.Google Scholar
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 Scholar
Shea, S.L., Doussard-Roosevelt, J.A. & Aslin, R.N. (1985). Pupillary measures of binocular luminance summation in infants and stereoblind adults. Investigative Ophthalmology and Visual Sciences 26, 1064–1070.Google Scholar
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., Kuchitwa, S. & Sukekawa, K. (1982). Two pupilloconstrictor areas in the occipital cortex of the cat. Brain Research 247, 134–137.CrossRefGoogle ScholarPubMed
Shoumura, K., Kuchdwa, S., Imai, H., Kuchhwa, T. & Kumakura, T. (1984). Cerebral cortical control of pupillary movements: anatomical and physiological studies in the cat. Asian Medical Journal 21, 16–33.Google Scholar
Sillito, A.M. (1968). The pretectal light input to the pupilloconstrictor neurons. Journal of Physiology 204, 36–37P.Google Scholar
Sireteanu, R. (1987). Binocular luminance summation in humans with defective binocular vision. Investigative Ophthalmology and Visual Sciences 28, 349–355.Google Scholar
Sireteanu, R. & Altmann, L. (1987). Binocular luminance summation in young kittens and adult strabismic cats. Investigative Ophthalmology and Visual Sciences 28, 343–348.Google Scholar
Steiger, H.J. & Buettner-Ennever, J.A. (1979). Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase. Brain Research 160, 1–15.CrossRefGoogle ScholarPubMed
Straschill, M. & Hoffmann, K.-P. (1969). Response characteristics of movement detecting neurons in pretectal region of the cat. Experimental Neurology 25, 165–176.Google Scholar
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.Google Scholar
Yoshioka, 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 of Psychiatry and Neurology ofJapan 11, 70–100.Google Scholar