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Connections between the zona incerta and superior colliculus in the monkey and squirrel

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Abstract

The zona incerta contains GABAergic neurons that project to the superior colliculus in the cat and rat, suggesting that it plays a role in gaze changes. However, whether this incertal connection represents a general mammalian pattern remains to be determined. We used neuronal tracers to examine the zona incerta connections with the midbrain tectum in the gray squirrel and macaque monkey. Collicular injections in both species revealed that most incertotectal neurons lay in the ventral layer, but anterogradely labeled tectoincertal terminals were found in both the dorsal and ventral layers. In the monkey, injections of the pretectum also produced retrograde labeling, but mainly in the dorsal layer. The dendritic fields of incertotectal and incertopretectal cells were generally contained within the layer inhabited by their somata. The macaque, but not the squirrel, zona incerta extended dorsolaterally, within the external medullary lamina. Zona incerta injections produced retrogradely labeled neurons in the superior colliculus of both species. In the squirrel, most cells inhabited the lower sublamina of the intermediate gray layer, but in the monkey, they were scattered throughout the deeper layers. Labeled cells were present among the pretectal nuclei in both species. Labeled terminals were concentrated in the lower sublamina of the intermediate gray layer of both species, but were dispersed among the pretectal nuclei. In summary, an incertal projection that is concentrated on the collicular motor output layers and that originates in the ventral layer of the ipsilateral zona incerta is a common mammalian feature, suggesting an important role in collicular function.

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Abbreviations

III:

Oculomotor nucleus

APt:

Anterior pretectal nucleus

BDA:

Biotinylated dextran amine

BP:

Basilar pons

DLG:

Dorsal lateral geniculate nucleus

EML:

External medullary lamina

GP:

Globus pallidus

HRP:

Horseradish peroxidase

IC:

Inferior colliculus

ICa:

Internal capsule

Lim:

Nucleus limitans

MG:

Medial geniculate nucleus

MPt:

Medial pretectal nucleus

nPC:

Nucleus of the posterior commissure

nOT:

Nucleus of the optic tract

Opt:

Stratum opticum

OT:

Optic tract

PAG:

Periaqueductal gray

PB:

Parabrachial nucleus

PG:

Pregeniculate

Pul:

Pulvinar

Pt:

Pretectum

PPt:

Posterior pretectal nucleus

RT:

Reticular thalamic nucleus

SAI:

Intermediate white layer

SC:

Superior colliculus

SGS:

Stratum griseum superficiale

SGI:

Stratum griseum intermediale

lSGI:

SGI, lower sublamina

uSGI:

SGI, upper sublamina

SGP:

Stratum griseum profundum

SNc:

Substantia nigra pars compacta

SNl:

Substantia nigra pars lateralis

SNr:

Substantia nigra pars reticulata

SO:

Stratum opticum

STh:

Subthalamic nucleus

WGA-HRP:

Wheat germ agglutinin conjugated HRP

VLG:

Ventral lateral geniculate nucleus

VP:

Ventral posterior nucleus

ZI:

Zona incerta

dZI:

Dorsal layer of ZI

vZI:

Ventral layer of ZI

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Acknowledgements

This manuscript is dedicated to the memory of Dr. Rick Chia-Sheng Lin, whose infectious enthusiasm for the zona incerta and all his other interests will be sorely missed. We would also like to thank Drs. Susan Warren, Kimberly Simpson and William C. Hall for their thoughtful readings of earlier versions of this work. This work was supported by the National Eye Institute of Health Grant #EY019663 to MAB and PJM.

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  1. Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, MS, 39216, USA

    Paul J. May

  2. Department of Ophthalmology, University of Mississippi Medical Center, Jackson, MS, 39216, USA

    Paul J. May

  3. Department of Neurology, University of Mississippi Medical Center, Jackson, MS, 39216, USA

    Paul J. May

  4. Fuster Laboratory of Cognitive Neuroscience, Department of Psychiatry and Biobehavioral Sciences and Neurobiology, Semel Institute for Neuroscience and Human Behavior, University of California at Los Angeles, Los Angeles, CA, 90095, USA

    Michele A. Basso

  5. Brain Research Institute, David Geffen School of Medicine, University of California at Los Angeles, Los Angeles, CA, 90095, USA

    Michele A. Basso

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  1. Paul J. May
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  2. Michele A. Basso
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Correspondence to Paul J. May.

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May, P.J., Basso, M.A. Connections between the zona incerta and superior colliculus in the monkey and squirrel. Brain Struct Funct 223, 371–390 (2018). https://doi.org/10.1007/s00429-017-1503-2

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  • DOI: https://doi.org/10.1007/s00429-017-1503-2

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