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Pupillary light reflex circuits in the Macaque Monkey: the olivary pretectal nucleus

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Abstract

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.

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Abbreviations

At:

Axon terminal

At*:

Labeled axon terminal

BDA:

Biotinylated dextran amine

CC:

Caudal central subdivision

CG:

Central gray

Den:

Dendrite

Den*:

Labeled dendrite

DLG:

Dorsal lateral geniculate nucleus

DR:

Dorsal raphe

EWpg:

Preganglionic Edinger-Westphal nucleus

IC:

Inferior colliculus

III:

Oculomotor nucleus

InC:

Interstitial nucleus of Cajal

IV:

Trochlear nucleus

MD:

Medial dorsal nucleus

MG:

Medial geniculate nucleus

MLF:

Medial longitudinal fasciculus

MPt:

Medial pretectal nucleus

MRF:

Midbrain reticular formation

nOT:

Nucleus of the optic tract

nPC:

Nucleus of the posterior commissure

OPt:

Olivary pretectal nucleus

P:

Pyramid

PAG:

Periaqueductal gray

PC:

Posterior commissure

PhaL:

Phaseolus vulgaris leucoagglutinin

PRF:

Pontine reticular formation

PPT:

Posterior pretectal nucleus

Pt:

Pretectum

Pul:

Pulvinar

SGI:

Intermediate gray layer

SGP:

Deep gray layer

SN:

Substantia nigra

SOA:

Supraoculomotor area

Soma*:

Labeled soma

WGA-HRP:

Wheat germ agglutinin conjugated horseradish peroxidase

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Acknowledgements

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.

Funding

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.

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Authors and Affiliations

  1. Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, 2500 N. State St, Jackson, MS, 39202, USA

    Paul J. May & Susan Warren

  2. Department of Ophthalmology, University of Mississippi Medical Center, Jackson, MS, USA

    Paul J. May

  3. Department of Neurology, University of Mississippi Medical Center, Jackson, MS, USA

    Paul J. May

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  1. Paul J. May
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  2. Susan Warren
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Contributions

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.

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Correspondence to Paul J. May.

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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).

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May, P.J., Warren, S. Pupillary light reflex circuits in the Macaque Monkey: the olivary pretectal nucleus. Brain Struct Funct 225, 305–320 (2020). https://doi.org/10.1007/s00429-019-02003-7

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