Pupillary light reflex circuits in the Macaque Monkey: the olivary pretectal nucleus
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The olivary pretectal nucleus is the first central connection in the pupillary light reflex pathway, the circuit that adjusts the diameter of the pupil in response to ambient light levels. This study investigated aspects of the morphology and connectivity of the olivary pretectal nucleus in macaque monkeys by use of anterograde and retrograde tracers. Within the pretectum, the vast majority of neurons projecting to the preganglionic Edinger–Westphal nucleus were found within the olivary pretectal nucleus. Most of these neurons had somata located at the periphery of the nucleus and their heavily branched dendrites extended into the core of the nucleus. Retinal terminals were concentrated within the borders of the olivary pretectal nucleus. Ultrastructural examination of these terminals showed that they had clear spherical vesicles, occasional dense-core vesicles, and made asymmetric synaptic contacts. Retrogradely labeled cells projecting to the preganglionic Edinger–Westphal nucleus displayed relatively few somatic contacts. Double labeling indicated that these neurons receive direct retinal input. The concentration of retinal terminals within the nucleus and the extensive dendritic trees of the olivary projection cells provide a substrate for very large receptive fields. In some species, pretectal commissural connections are a substrate for balancing the direct and consensual pupillary responses to produce pupils of equal size. In the macaque, there was little evidence for such a commissural projection based on either anterograde or retrograde tracing. This may be due to the fact that each macaque retina provides nearly equal density projections to the ipsilateral and contralateral olivary pretectal nucleus.
KeywordsRetinal projections Pupil Autonomic Luminance Midbrain
Labeled axon terminal
Biotinylated dextran amine
Caudal central subdivision
Dorsal lateral geniculate nucleus
Preganglionic Edinger-Westphal nucleus
Interstitial nucleus of Cajal
Medial dorsal nucleus
Medial geniculate nucleus
Medial longitudinal fasciculus
Medial pretectal nucleus
Midbrain reticular formation
Nucleus of the optic tract
Nucleus of the posterior commissure
Olivary pretectal nucleus
Phaseolus vulgaris leucoagglutinin
Pontine reticular formation
Posterior pretectal nucleus
Intermediate gray layer
Deep gray layer
Wheat germ agglutinin conjugated horseradish peroxidase
We would like to thank Ms. Malinda Danielson, Jinrong Wei, and Olga Golanov for their technical assistance with respect to surgeries and processing of the brains, as well as preparation of the figures. We are also indebted to Mr. Glen Hoskins for processing and cutting tissue for electron microscopy.
PJM helped to: design the experiments, carry out the experiments, analyze the data, write the manuscript, and edit the manuscript. SW helped to: carry out the experiments, analyze the data, and edit the manuscript.
Portions of the material presented here were supported by funds from National Institute of Health grants: EY07166 to Paul J. May, EY014263 to Paul J. May, Paul D.R. Gamlin, and Susan Warren, and National Science Foundation Grant IBN-0130954 to Martha Bickford and Paul J. May.
Compliance with ethical standards
Conflict of interest
Neither author has any perceived or real conflicts of interest with respect to this submission.
Ethical use of animals statement
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution at which the studies were conducted. Specifically, they were undertaken under protocols approved by the Institutional Animal Care and Use Committee of the University of Mississippi Medical Center (USDA Animal Welfare Assurance # D16-00174).
- Barnerssoi M, May PJ (2016) Postembedding immunohistochemistry for inhibitory neurotransmitters in conjunction with neuroanatomical tracers. In: Van Bockstaele EJ (ed) Transmission electron microscopy methods for understanding the brain. Neuromethods, vol 115. Springer Science, New York, pp 181–203Google Scholar
- Clarke RJ, Blanks RH, Giolli RA (2003a) Midbrain connections of the olivary pretectal nucleus in the marmoset (Callithrix jacchus): implications for the pupil light reflex pathway. Anat Embryol (Berl) 207:149–155Google Scholar
- Gamlin PD, Clarke RJ (1995) The pupillary light reflex pathway of the primate. J Am Opt Assoc 66:415–418Google Scholar
- Gerfen CR, Sawchenko PE (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris leucoagglutinin (PHA-L). Brain Res 290:219–238PubMedPubMedCentralGoogle Scholar
- May PJ, Sun W, Erichsen JT (2008) Defining the pupillary component of the perioculomotor preganglionic population within a unitary primate Edinger-Westphal nucleus. In: Kennard C, Leigh RJ (eds) Using eye movements as an experimental probe of brain function, Prog Brain Res, vol 171, pp 97–106Google Scholar
- May P J, Reiner A, Gamlin PD (2019) Autonomic regulation of the eye. In: Encyclopedia of neuroendocrine and autonomic systems. In: Nelson R (ed). Oxford University Press, OxfordGoogle Scholar
- Miguel-Hildago JJ, Senba E, Takatsuji K, Tohyama M (1994) Projections of takykinin- and glutaminase-containing rat retinal ganglion cells. Brain Res Bul 35:73–84Google Scholar
- Sun W, May PJ (1995) Morphology and connections of the pupillary light reflex pathway in cat and monkey. Invest Ophthal Vis Sci 36:S12Google Scholar