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Superior colliculus projections to target populations in the supraoculomotor area of the macaque monkey

Published online by Cambridge University Press:  11 November 2021

Paul J. May Open the ORCID record for Paul J. May [Opens in a new window] ,
Martin O. Bohlen ,
Eddie Perkins ,
Niping Wang  and
Susan Warren
Paul J. May*
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, Mississippi
Martin O. Bohlen
Affiliation:
Department of Biomedical Engineering, Duke University, Durham, North Carolina
Eddie Perkins
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, Mississippi Department of Neurosurgery, University of Mississippi Medical Center, Jackson, Mississippi
Niping Wang
Affiliation:
Department of Periodontics and Preventive Sciences, School of Dentistry, University of Mississippi Medical Center, Jackson, Mississippi
Susan Warren
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, Mississippi
*
*Corresponding author: Paul J. May, email: [email protected]
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Abstract

A projection by the superior colliculus to the supraoculomotor area (SOA) located dorsal to the oculomotor complex was first described in 1978. This projection’s targets have yet to be identified, although the initial study suggested that vertical gaze motoneuron dendrites might receive this input. Defining the tectal targets is complicated by the fact the SOA contains a number of different cell populations. In the present study, we used anterograde tracers to characterize collicular axonal arbors and retrograde tracers to label prospective SOA target populations in macaque monkeys. Close associations were not found with either superior or medial rectus motoneurons whose axons supply singly innervated muscle fibers. S-group motoneurons, which supply superior rectus multiply innervated muscle fibers, appeared to receive a very minor input, but C-group motoneurons, which supply medial rectus multiply innervated muscle fibers, received no input. A number of labeled boutons were observed in close association with SOA neurons projecting to the spinal cord, or the reticular formation in the pons and medulla. These descending output neurons are presumed to be peptidergic cells within the centrally projecting Edinger–Westphal population. It is possible the collicular input provides a signaling function for neurons in this population that serve roles in either stress responses, or in eating and drinking behavior. Finally, a number of close associations were observed between tectal terminals and levator palpebrae superioris motoneurons, suggesting the possibility that the superior colliculus provides a modest direct input for raising the eyelids during upward saccades.

Keywords

oculomotorEdinger–Westphalurocortineyelidextraocular musclelevator palpebrae superioris
Type
Research Article
Information
Visual Neuroscience , Volume 38 , 2021 , E017
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Copyright
© The Author(s), 2021. Published by Cambridge University Press

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References

Adamczyk, C., Strupp, M., Jahn, K. & Horn, A.K. ( 2015 ). Calretinin as a marker for premotor neurons involved in upgaze in human brainstem. Frontiers in Neuroanatomy 9, 153. https://doi.org/10.3389/fnana.2015.00153CrossRefGoogle ScholarPubMed
Ahlfeld, J., Mustari, M. & Horn, A.K. ( 2011 ). Sources of calretinin inputs to motoneurons of extraocular muscles involved in upgaze. Annals of the New York Academy of Sciences 1233, 91–99. http://dx.doi.org/10.1111/j.1749-6632.2011.06168.xCrossRefGoogle ScholarPubMed
Becker, W. & Fuchs, A.F. ( 1988 ). Lid-eye coordination during vertical gaze changes in man and monkey. Journal of Neurophysiology 60, 1227–1252. http://dx.doi.org/10.1152/jn.1988.60.4.1227CrossRefGoogle ScholarPubMed
Behan, M. ( 1985 ). An EM-autoradiographic and EM-HRP study of the commissural projection of the superior colliculus in the cat. Journal of Comparative Neurology 234, 105–116. http://dx.doi.org/10.1002/CNE.902340108CrossRefGoogle ScholarPubMed
Behan, M. & Kime, N.M. ( 1996 ). Spatial distribution of tectotectal connections in the cat. Progress in Brain Research 112, 131–142. http://dx.doi.org/10.1016/s0079-6123(08)63325-7CrossRefGoogle ScholarPubMed
Bohlen, M.O., Gamlin, P.D., Warren, S. & May, P.J. ( 2021 ). Cerebellar projections to the macaque midbrain tegmentum: Possible near response connections. Visual Neuroscience 39, E0007.Google Scholar
Bohlen, M.O., Warren, S. & May, P.J. ( 2016 ). A central mesencephalic reticular formation projection to the supraoculomotor area in macaque monkeys. Brain Structure & Function 221, 2209–2229. http://dx.doi.org/10.1007/s00429-015-1039-2CrossRefGoogle ScholarPubMed
Bondi, A.Y. & Chiarandini, D.J. ( 1983 ). Morphologic and electrophysiologic identification of multiply innervated fibers in rat extraocular muscles. Investigative Ophthalmology & Visual Science 24, 516–519.Google ScholarPubMed
Büttner-Ennever, J.A. & Akert, K. ( 1981 ). Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey. Journal of Comparative Neurology 197, 17–27. https://doi.org/10.1002/cne.901970103CrossRefGoogle ScholarPubMed
Büttner-Ennever, J.A., Horn, A.K., Henn, V. & Cohen, B. ( 1999 ). Projections from the superior colliculus motor map to omnipause neurons in monkey. Journal of Comparative Neurology 413, 55–67. https://doi.org/10.1002/(sici)1096-9861(19991011)413:1<55::aid-cne3>3.0.co;2-k3.0.CO;2-K>CrossRefGoogle ScholarPubMed
Büttner-Ennever, J.A., Horn, A.K., Scherberger, H. & D’Ascanio, P. ( 2001 ). Motoneurons of twitch and nontwitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys. Journal of Comparative Neurology 438, 318–335. http://dx.doi.org/10.1002/cne.1318CrossRefGoogle ScholarPubMed
Castiglioni, A.J., Gallaway, M.C. & Coulter, J.D. ( 1978 ). Spinal projections from the midbrain in monkey. Journal of Comparative Neurology 178, 329–346. http://dx.doi.org/10.1002/cne.901780208CrossRefGoogle ScholarPubMed
Chaturvedi, V. & van Gisbergen, J.A. ( 1999 ). Perturbation of combined saccade-vergence movements by microstimulation in monkey superior colliculus. Journal of Neurophysiology 81, 2279–2296. http://dx.doi.org/10.1152/jn.1999.81.5.2279CrossRefGoogle ScholarPubMed
Chaturvedi, V & Van Gisbergen, J.A. ( 2000 ). Stimulation in the rostral pole of monkey superior colliculus: Effects on vergence eye movements. Experimental Brain Research 132, 72–78. http://dx.doi.org/10.1007/s002219900221CrossRefGoogle ScholarPubMed
Che Ngwa, E., Zeeh, C., Messoudi, A., Büttner-Ennever, J.A. & Horn, A.K.E. ( 2014 ). Delineation of motoneuron subgroups supplying individual eye muscles in the human oculomotor nucleus. Frontiers in Neuroanatomy 8, 2. https://doi.org/10.3389/fnana.2014.00002CrossRefGoogle ScholarPubMed
Chen, B. & May, P.J. ( 2002 ). Premotor circuits controlling eyelid movements in conjunction with vertical saccades in the cat: I. The rostral interstitial nucleus of the medial longitudinal fasciculus. Journal of Comparative Neurology 450, 183–202. https://doi.org/10.1002/cne.10313CrossRefGoogle ScholarPubMed
Chen, B. & May, P.J. ( 2007 ). Premotor circuits controlling eyelid movements in conjunction with vertical saccades in the cat: II. Interstitial nucleus of Cajal. Journal of Comparative Neurology 500, 676–692. http://dx.doi.org/10.1002/cne.21203CrossRefGoogle ScholarPubMed
Chiarandini, D.J. & Stefani, E. ( 1979 ). Electrophysiological identification of two types of fibres in rat extraocular muscles. Journal of Physiology 290, 453–465. http://dx.doi.org/10.1113/jphysiol.1979.sp012783CrossRefGoogle ScholarPubMed
Chung, R.Y., Mason, P., Strassman, A. & Maciewicz, R. ( 1987 ). Edinger–Westphal nucleus: Cells that project to spinal cord contain corticotropin-releasing factor. Neuroscience Letters 83, 13–19. http://dx.doi.org/10.1016/0304-3940(87)90208-4CrossRefGoogle ScholarPubMed
Comoli, E., Das Neves Favaro, P., Vautrelle, N., Leriche, M., Overton, P.G. & Redgrave, P. ( 2012 ). Segregated anatomical input to sub-regions of the rodent superior colliculus associated with approach and defense. Frontiers in Neuroanatomy 6, 9. https://doi.org/10.3389/fnana.2012.00009CrossRefGoogle ScholarPubMed
Cowie, R.J., Smith, M.K. & Robinson, D.L. ( 1994 ). Subcortical contributions to head movements in macaques. II. Connections of a medial pontomedullary head-movement region. Journal of Neurophysiology 72, 2665–2682. http://dx.doi.org/10.1152/jn.1994.72.6.2665CrossRefGoogle ScholarPubMed
Cullen, K.E. & Van Horn, M.R. ( 2011 ). The neural control of fast vs. slow vergence eye movements. European Journal of Neuroscience 33, 2147–2154. http://dx.doi.org/10.1111/j.1460-9568.2011.07692.x.CrossRefGoogle ScholarPubMed
Das, V.E. ( 2011 ). Cells in the supraoculomotor area in monkeys with strabismus show activity related to the strabismus angle. Annals of the New York Academy of Science 1233, 85–90.CrossRefGoogle ScholarPubMed
Edwards, S.B. ( 1977 ). The commissural projection of the superior colliculus in the cat. Journal of Comparative Neurology 173, 23–40. https://doi.org/10.1002/cne.901730103CrossRefGoogle ScholarPubMed
Edwards, S.B. & Henkel, C.K. ( 1978 ). Superior colliculus connections with the extraocular motor nuclei in the cat. Journal of Comparative Neurology 179, 451–467. http://dx.doi.org/10.1002/cne.901790212CrossRefGoogle ScholarPubMed
Erichsen, J.T. & May, P.J. ( 2012 ). A perioculomotor nitridergic population in the macaque and cat. Investigative Ophthalmology & Visual Science 53, 5751–5761. http://dx.doi.org/10.1167/iovs.12-10287CrossRefGoogle Scholar
Evinger, C., Graf, W.M. & Baker, R. ( 1987 ). Extra- and intracellular HRP analysis of the organization of extraocular motoneurons and internuclear neurons in the Guinea pig and rabbit. Journal of Comparative Neurology 262, 429–445. http://dx.doi.org/10.1002/cne.902620307CrossRefGoogle ScholarPubMed
Evinger, C., Manning, K.A. & Sibony, P.A. ( 1991 ). Eyelid movements. Mechanisms and normal data. Investigative Ophthalmology and Visual Science 32, 387–400.Google ScholarPubMed
Fuchs, A.F., Becker, W., Ling, L., Langer, T.P. & Kaneko, C.R. ( 1992 ). Discharge patterns of levator palpebrae superioris motoneurons during vertical lid and eye movements in the monkey. Journal of Neurophysiology 68, 233–243. http://dx.doi.org/10.1152/jn.1992.68.1.233CrossRefGoogle ScholarPubMed
Furigo, I.C., de Oliveira, W.F., de Oliveira, A.R., Comoli, E., Baldo, M.V.C., Mota-Ortiz, S.R. & Canteras, N.S. ( 2010 ). The role of the superior colliculus in predatory hunting. Neuroscience 165, 1–15. https://doi.org/10.1016/j.neuroscience.2009.10.004CrossRefGoogle ScholarPubMed
Gaszner, B., Csernus, V. & Kozicz, T. ( 2004 ). Urocortinergic neurons respond in a differentiated manner to various acute stressors in the Edinger–Westphal nucleus in the rat. Journal of Comparative Neurology 480, 170–179. http://dx.doi.org/10.1002/cne.20343CrossRefGoogle Scholar
Gerfen, C.R. & Sawchenko, P.E. ( 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 Research 290, 219–238. http://dx.doi.org/10.1016/0006-8993(84)90940-5CrossRefGoogle Scholar
Grantyn, A. & Berthoz, A. ( 1977 ). Synaptic actions of the superior colliculus on medial rectus motoneurons in the cat. Neuroscience 2, 945–951. https://doi.org/10.1016/0306-4522(77)90117-8CrossRefGoogle Scholar
Grantyn, A., Brandi, A.-M., Dubayle, D., Graf, W., Ugolini, G., Hadjidimitrakis, K. & Moschovakis, A. ( 2002 ). Density gradients of trans-synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey. Journal of Comparative Neurology 451, 346–361. http://dx.doi.org/10.1002/cne.10353CrossRefGoogle ScholarPubMed
Grantyn, A. & Grantyn, R. ( 1982 ). Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Experimental Brain Research 46, 243–256. http://dx.doi.org/10.1007/BF00237182CrossRefGoogle ScholarPubMed
Grantyn, A.A. & Grantyn, R. ( 1976 ). Synaptic actions of tectofugal pathways on abducens motoneurons in the cat. Brain Research 105, 269–285. http://dx.doi.org/10.1016/0006-8993(76)90425-xCrossRefGoogle ScholarPubMed
Guitton, D., Simard, R. & Codère, F. ( 1991 ). Upper eyelid movements measured with a search coil during blinks and vertical saccades. Investigative Ophthalmology & Visual Science 32, 3298–3305.Google ScholarPubMed
Hafed, Z.M., Goffart, L. & Krauzlis, R.J. ( 2009 ). A neural mechanism for microsaccade generation in the primate superior colliculus. Science 323, 940–943. http://dx.doi.org/10.1126/science.1166112CrossRefGoogle ScholarPubMed
Hafed, Z.M. & Krauzlis, R.J. ( 2010 ). Microsaccadic suppression of visual bursts in the primate superior colliculus. Journal of Neuroscience 30, 9542–9547. http://dx.doi.org/10.1523/JNEUROSCI.1137-10.2010CrossRefGoogle ScholarPubMed
Harting, J.K., Huerta, M.F., Frankfurter, A.J., Strominger, N.L. & Royce, G.J. ( 1980 ). Ascending pathways from the monkey superior colliculus: An autoradiographic analysis. Journal of Comparative Neurology 192, 853–882. http://dx.doi.org/10.1002/cne.901920414CrossRefGoogle ScholarPubMed
Hepp, K., Henn, V., Vilis, T. & Cohen, B. ( 1989 ). Brainstem regions related to saccade generation. Reviews of Oculomotor Research 3, 105–212.Google ScholarPubMed
Hernández, R.G., Calvo, P.M., Blumer, R., de la Cruz, R.R. & Pastor, A.M. ( 2019 ). Functional diversity of motoneurons in the oculomotor system. Proceedings of the National Academy of Science U S A 116, 3837–3846. http://dx.doi.org/10.1073/pnas.1818524116CrossRefGoogle ScholarPubMed
Hess, A. & Pilar, G. ( 1963 ). Slow fibers in the extraocular muscles of the cat. Journal of Physiology 169, 780–798. http://dx.doi.org/10.1113/jphysiol.1963.sp007296CrossRefGoogle Scholar
Horn, A.K. & Büttner-Ennever, J.A. ( 2008 ). Brainstem circuits controlling lid-eye coordination in monkey. Progress in Brain Research 171, 87–95. https://doi.org/10.1016/S0079-6123(08)00612-2CrossRefGoogle ScholarPubMed
Horn, A.K., Büttner-Ennever, J.A., Gayde, M. & Messoudi, A. ( 2000 ). Neuroanatomical identification of mesencephalic premotor neurons coordinating eyelid with upgaze in the monkey and man. Journal of Comparative Neurology 420, 19–34. https://doi.org/10.1002/(sici)1096-9861(20000424)420:1<19::aid-cne2>3.0.co;2-d3.0.CO;2-D>CrossRefGoogle ScholarPubMed
Horn, A.K., Eberhorn, A., Härtig, W., Ardeleanu, P., Messoudi, A. & Büttner-Ennever, J.A. ( 2008 ). Perioculomotor cell groups in monkey and man defined by their histochemical and functional properties: Reappraisal of the Edinger–Westphal nucleus. Journal of Comparative Neurology 507, 1317–1335. http://dx.doi.org/10.1002/cne.21598CrossRefGoogle ScholarPubMed
Jacoby, J., Chiarandini, D.J. & Stefani, E. ( 1989 ). Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles. Journal of Neurophysiology 61, 116–125. http://dx.doi.org/10.1152/jn.1989.61.1.116CrossRefGoogle ScholarPubMed
Judge, S.J. & Cumming, B.G. ( 1986 ). Neurons in the monkey midbrain with activity related to vergence eye movement and accommodation. Journal of Neurophysiology 55, 915–930. http://dx.doi.org/10.1152/jn.1986.55.5.915CrossRefGoogle ScholarPubMed
Kozicz, T. ( 2010 ). The missing link; the significance of urocortin 1/urocortin 2 in the modulation of the dorsal raphe serotoninergic system. Molecular Psychiatry 15, 340–341. http://dx.doi.org/10.1038/mp.2009.134CrossRefGoogle ScholarPubMed
Kozicz, T., Bittencourt, J.C., May, P.J., Reiner, A., Gamlin, P.D., Palkovits, M., Horn, A.K., Toledo, C.A. & Ryabinin, A.E. ( 2011 ). The Edinger–Westphal nucleus: A historical, structural, and functional perspective on a dichotomous terminology. Journal of Comparative Neurology 519, 1413–1434. http://dx.doi.org/10.1002/cne.22580CrossRefGoogle ScholarPubMed
Kozicz, T., Li, M. & Arimura, A. ( 2001 ). The activation of urocortin immunoreactive neurons in the Edinger–Westphal nucleus following stress in rats. Stress 4, 85–90. https://doi.org/10.3109/10253890109115724CrossRefGoogle ScholarPubMed
Kozicz, T., Yanaihara, H. & Arimura, A. ( 1998 ). Distribution of urocortin-like immunoreactivity in the central nervous system of the rat. Journal of Comparative Neurology 391, 1–10. https://doi.org/10.1002/(sici)1096-9861(19980202)391:1<1::aid-cne1>3.0.co;2-63.0.CO;2-6>CrossRefGoogle ScholarPubMed
Krauzlis, R.J. ( 2003 ). Neuronal activity in the rostral superior colliculus related to the initiation of pursuit and saccadic eye movements. Journal of Neuroscience 23, 4333–4344. http://dx.doi.org/10.1523/JNEUROSCI.23-10-04333.2003CrossRefGoogle ScholarPubMed
Krauzlis, R.J., Lovejoy, L.J & Zénon, A. ( 2013 ). Superior colliculus and visual spatial attention. Annual Review of Neuroscience 36, 165–182. http://dx.doi.org/10.1146/annurev-neuro-062012-170249CrossRefGoogle ScholarPubMed
Langer, T., Kaneko, C.R., Scudder, C.A. & Fuchs, A.F. ( 1986 ). Afferents to the abducens nucleus in the monkey and cat. Journal of Comparative Neurology 245, 379–400. https://doi.org/10.1002/cne.902450307CrossRefGoogle Scholar
Langer, T.P. & Kaneko, C.R. ( 1990 ). Brainstem afferents to the oculomotor omnipause neurons in monkey. Journal of Comparative Neurology 295, 413–427. http://dx.doi.org/10.1002/cne.902950306CrossRefGoogle ScholarPubMed
Maciewicz, R., Phipps, B.S., Foote, W.E., Aronin, N. & DiFiglia, M. ( 1983 ). The distribution of substance P-containing neurons in the cat Edinger–Westphal nucleus: Relationship to efferent projection systems. Brain Research 270, 217–230. http://dx.doi.org/10.1016/0006-8993(83)90595-4CrossRefGoogle ScholarPubMed
Maciewicz, R., Phipps, B.S., Grenier, J. & Poletti, C.E. ( 1984 ). Edinger–Westphal nucleus: Cholecystokinin immunocytochemistry and projections to spinal cord and trigeminal nucleus in the cat. Brain Research 299, 139–145. http://dx.doi.org/10.1016/0006-8993(84)90796-0CrossRefGoogle ScholarPubMed
Maciewicz, R.J., Kaneko, C.R., Highstein, S.M. & Baker, R. ( 1975 ). Morphophysiological identification of interneurons in the oculomotor nucleus that project to the abducens nucleus in the cat. Brain Research 96, 60–65. http://dx.doi.org/10.1016/0006-8993(75)90571-5CrossRefGoogle ScholarPubMed
May, P.J., Baker, H., Vidal, P.P., Spencer, R.F. & Baker, R. ( 1987 ). Morphology and distribution of serotoninergic and oculomotor internuclear neurons in the cat midbrain. Journal of Comparative Neurology 266, 150–170. http://dx.doi.org/10.1002/cne.902660203CrossRefGoogle ScholarPubMed
May, P.J. & Porter, J.D. ( 1992 ). The laminar distribution of macaque tectobulbar and tectospinal neurons. Visual Neuroscience 8, 257–276. http://dx.doi.org/10.1017/s0952523800002911CrossRefGoogle ScholarPubMed
May, P.J., Reiner, A.J. & Ryabinin, A.E. ( 2008 ). Comparison of the distributions of urocortin-containing and cholinergic neurons in the perioculomotor midbrain of the cat and macaque. Journal of Comparative Neurology 507, 1300–1316. http://dx.doi.org/10.1002/cne.21514CrossRefGoogle Scholar
May, P.J., Vidal, P.P., Baker, H. & Baker, R. ( 2012 ). Physiological and anatomical evidence for an inhibitory trigemino-oculomotor pathway in the cat. Journal of Comparative Neurology 520, 2218–2240. http://dx.doi.org/10.1002/cne.23039CrossRefGoogle ScholarPubMed
May, P.J., Warren, S., Gamlin, P.D.R. & Billig, I. ( 2018 ). An anatomic characterization of the midbrain near response neurons in the macaque monkey. Investigative Ophthalmology & Visual Science 59, 1486–1502. https://doi.org/10.1167/iovs.17-23737CrossRefGoogle ScholarPubMed
Mays, L.E. ( 1984 ). Neural control of vergence eye movements: Convergence and divergence neurons in midbrain. Journal of Neurophysiology 51, 1091–1108. https://doi.org/10.1152/jn.1984.51.5.1091CrossRefGoogle ScholarPubMed
McCrea, R.M., Strassman, A. & Highstein, S.M. ( 1986 ). Morphology and physiology of abducens motoneurons and internuclear neurons intracellularly injected with horseradish peroxidase in alert squirrel monkeys. Journal of Comparative Neurology 243, 291–308. https://doi.org/10.1002/cne.902430302CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. ( 1988a ). Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. Journal of Neurophysiology 60, 232–262. http://dx.doi.org/10.1152/jn.1988.60.1.232CrossRefGoogle Scholar
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. ( 1988b ). Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. Journal of Neurophysiology 60, 263–302. https://doi.org/10.1152/jn.1988.60.1.263CrossRefGoogle Scholar
Moschovakis, A.K., Kitama, T., Dalezios, Y., Petit, J., Brandi, A.M. & Grantyn, A.A. ( 1998 ). An anatomical substrate for the spatiotemporal transformation. Journal of Neuroscience 18, 10219–10229. http://dx.doi.org/10.1523/JNEUROSCI.18-23-10219.1998CrossRefGoogle ScholarPubMed
Munoz, D.P. & Istvan, P.J. ( 1998 ). Lateral inhibitory interactions in the intermediate layers of the monkey superior colliculus. Journal of Neurophysiology 79, 1193–1209. http://dx.doi.org/10.1152/jn.1998.79.3.1193CrossRefGoogle ScholarPubMed
Munoz, D.P. & Wurtz, R.H. ( 1993a ). Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. Journal of Neurophysiology 70, 559–575. http://dx.doi.org/10.1152/jn.1993.70.2.559CrossRefGoogle Scholar
Munoz, D.P. & Wurtz, R.H. ( 1993b ). Fixation cells in monkey superior colliculus. II. Reversible activation and deactivation. Journal of Neurophysiology 70, 576–589. http://dx.doi.org/10.1152/jn.1993.70.2.576CrossRefGoogle Scholar
Nelson, J.S., Goldberg, S.J. & McClung, J.R. ( 1986 ). Motoneuron electrophysiological and muscle contractile properties of superior oblique motor units in cat. Journal of Neurophysiology 55, 715–726. http://dx.doi.org/10.1152/jn.1986.55.4.715CrossRefGoogle ScholarPubMed
Ohtsuka, K. & Nagasaka, Y. ( 1999 ). Divergent axon collaterals from the rostral superior colliculus to the pretectal accommodation-related areas and the omnipause neuron area in the cat. Journal of Comparative Neurology 413, 68–76. https://doi.org/10.1002/(sici)1096-9861(19991011)413:1<68::aid-cne4>3.0.co;2-73.0.CO;2-7>CrossRefGoogle ScholarPubMed
Ohtsuka, K. & Sato, A. ( 1997 ). Retinal projections to the accommodation-related area in the rostral superior colliculus of the cat. Experimental Brain Research 113, 169–173. http://dx.doi.org/10.1007/BF02454154CrossRefGoogle ScholarPubMed
Olivier, E., Porter, J.D. & May, P.J. ( 1998 ). Comparison of the distribution and somatodendritic morphology of tectotectal neurons in the cat and monkey. Visual Neuroscience 15, 903–922. http://dx.doi.org/10.1017/s095252389815513xCrossRefGoogle Scholar
Pallus, A.C., Walton, M.M.G. & Mustari, M.J. ( 2018 ). Response of supraoculomotor area neurons during combined saccade-vergence movements. Journal of Neurophysiology 119, 585–596.CrossRefGoogle ScholarPubMed
Pasik, T., Pasik, P. & Bender, M.B. ( 1966 ). The superior colliculi and eye movements. An experimental study in the monkey. Archives of Neurology 15, 420–436. http://dx.doi.org/10.1001/archneur.1966.00470160086012CrossRefGoogle ScholarPubMed
Peck, C.K. & Baro, J.A. ( 1997 ). Discharge patterns of neurons in the rostral superior colliculus of cat: Activity related to fixation of visual and auditory targets. Experimental Brain Research 113, 291–302. https://doi.org/10.1007/BF02450327CrossRefGoogle ScholarPubMed
Perkins, E., Warren, S. & May, P.J. ( 2009 ). The mesencephalic reticular formation as a conduit for primate collicular gaze control: Tectal inputs to neurons targeting the spinal cord and medulla. Anatomical Record 292, 1162–1181. http://dx.doi.org/10.1002/ar.20935CrossRefGoogle ScholarPubMed
Phipps, B.S., Maciewicz, R., Sandrew, B.B., Poletti, C.E. & Foote, W.E. ( 1983 ). Edinger–Westphal neurons that project to spinal cord contain substance P. Neuroscience Letters 36, 125–131. http://dx.doi.org/10.1016/0304-3940(83)90253-7CrossRefGoogle ScholarPubMed
Porter, J.D., Burns, L.A. & May, P.J. ( 1989 ). Morphological substrate for eyelid movements: Innervation and structure of primate levator palpebrae superioris and orbicularis oculi muscles. Journal of Comparative Neurology 287, 64–81. https://doi.org/10.1002/cne.902870106CrossRefGoogle ScholarPubMed
Robertson, B. & Grant, G. ( 1985 ). A comparison between wheat germ agglutinin-and choleragenoid-horseradish peroxidase as anterogradely transported markers in central branches of primary sensory neurones in the rat with some observations in the cat. Neuroscience 14, 895–905. https://doi.org/10.1016/0306-4522(85)90152-6CrossRefGoogle ScholarPubMed
Ryabinin, A.E. & Weitemier, A.Z. ( 2006 ). The urocortin 1 neurocircuit: Ethanol-sensitivity and potential involvement in alcohol consumption. Brain Research Reviews 52, 368–380. http://dx.doi.org/10.1016/j.brainresrev.2006.04.007CrossRefGoogle ScholarPubMed
Sato, A. & Ohtsuka, K. ( 1996 ). Projection from the accommodation-related area in the superior colliculus of the cat. Journal of Comparative Neurology 367, 465–476. http://10.0.3.234/(SICI)1096-9861(19960408)367:3<465::AID-CNE11>3.0.CO;2-G3.0.CO;2-G>CrossRefGoogle ScholarPubMed
Sibony, P.A., Evinger, C. & Manning, K.A. ( 1991 ). Eyelid movements in facial paralysis. Archives of Ophthalmology 109, 1555–1561. http://dx.doi.org/10.1001/ARCHOPHT.1991.01080110091043CrossRefGoogle ScholarPubMed
Sparks, D.L. & Hartwich-Young, R. ( 1989 ). The deep layers of the superior colliculus. Reviews of Oculomotor Research 3, 213–255.Google ScholarPubMed
Spencer, R.F. & Porter, J.D. ( 2006 ). Biological organization of the extraocular muscles. Progress in Brain Research 151, 43–80. https://doi.org/10.1016/S0079-6123(05)51002-1CrossRefGoogle ScholarPubMed
Spina, M., Merlo-Pich, E., Chan, R.K., Basso, A.M., Rivier, J., Vale, W. & Koob, G.F. ( 1996 ). Appetite-suppressing effects of urocortin, a CRF-related neuropeptide. Science 273, 1561–1564. http://dx.doi.org/10.1126/science.273.5281.1561CrossRefGoogle ScholarPubMed
Suzuki, S., Suzuki, Y. & Ohtsuka, K. ( 2004 ). Convergence eye movements evoked by microstimulation of the rostral superior colliculus in the cat. Neuroscience Research 49, 39–45. https://doi.org/10.1016/j.neures.2004.01.009CrossRefGoogle ScholarPubMed
Takahashi, M., Sugiuchi, Y., Izawa, Y. & Shinoda, Y. ( 2005 ). Commissural excitation and inhibition by the superior colliculus in tectoreticular neurons projecting to omnipause neuron and inhibitory burst neuron regions. Journal of Neurophysiology, 94, 1707–1726. http://dx.doi.org/10.1152/jn.00347.2005CrossRefGoogle ScholarPubMed
Ugolini, G., Klam, F., Doldan Dans, M., Dubayle, D., Brandi, A.M., Büttner-Ennever, J. & Graf, W. ( 2006 ). Horizontal eye movement networks in primates as revealed by retrograde transneuronal transfer of rabies virus: Differences in monosynaptic input to “slow” and “fast” abducens motoneurons. Journal of Comparative Neurology 498, 762–785. http://dx.doi.org/10.1002/cne.21092CrossRefGoogle ScholarPubMed
Upadhyaya, S. & Das, V.E. ( 2019 ). Response properties of cells within the rostral superior colliculus of strabismic monkeys. Investigative Ophthalmology & Visual Science 60, 4292–4302. https://doi.org/10.1167/iovs.19-27786CrossRefGoogle ScholarPubMed
Van Horn, M.R., Waitzman, D.M. & Cullen, K.E. ( 2013 ). Vergence neurons identified in the rostral superior colliculus code smooth eye movements in 3D space. Journal of Neuroscience 33, 7274–7284. http://dx.doi.org/10.1523/JNEUROSCI.2268-12.2013CrossRefGoogle ScholarPubMed
Vasconcelos, L.A., Donaldson, C., Sita, L.V., Casatti, C.A., Lotfi, C.F., Wang, L., Cadinouche, M.Z., Frigo, L., Elias, C.F., Lovejoy, D.A. & Bittencourt, J.C. ( 2003 ). Urocortin in the central nervous system of a primate (Cebus apella): Sequencing, immunohistochemical, and hybridization histochemical characterization. Journal of Comparative Neurology 463, 157–175. http://dx.doi.org/10.1002/cne.10742CrossRefGoogle ScholarPubMed
Vetter, D.E., Li, C., Zhao, L., Contarino, A., Liberman, M.C., Smith, G.W., Marchuk, Y., Koob, G.F., Heinemann, S.F., Vale, W. & Lee, K.F. ( 2002 ). Urocortin-deficient mice show hearing impairment and increased anxiety-like behavior. Nature Genetics 31, 363–369. http://dx.doi.org/10.1038/ng914CrossRefGoogle ScholarPubMed
Walton, M.M. & Mays, L.E. ( 2003 ). Discharge of saccade-related superior colliculus neurons during saccades accompanied by vergence. Journal of Neurophysiology 90, 1124–1139. http://dx.doi.org/10.1152/jn.00877.2002CrossRefGoogle ScholarPubMed
Wang, C.A., Boehnke, S.E., White, B.J. & Munoz, D.P. ( 2012 ). Microstimulation of the monkey superior colliculus induces pupil dilation without evoking saccades. Journal of Neuroscience 32, 3629–3636. http://dx.doi.org/10.1523/JNEUROSCI.5512-11.2012.CrossRefGoogle ScholarPubMed
Wang, C.A. & Munoz, D.P. ( 2018 ). Neural basis of location-specific pupil luminance modulation. Proceedings of the National Academy of Science U S A 115, 10446–10451. https://doi.org/10.1073/pnas.1809668115CrossRefGoogle ScholarPubMed
Wang, L., Martínez, V., Vale, W. & Taché, Y. ( 2000 ). Fos induction in selective hypothalamic neuroendocrine and medullary nuclei by intravenous injection of urocortin and corticotropin-releasing factor in rats. Brain Research 855, 47–57. https://doi.org/10.1016/s0006-8993(99)02200-3CrossRefGoogle ScholarPubMed
Wang, N., Perkins, E., Zhou, L., Warren, S. & May, P.J. ( 2013 ). Anatomical evidence that the superior colliculus controls saccades through central mesencephalic reticular formation gating of omnipause neuron activity. Journal of Neuroscience 33, 16285–16296. http://dx.doi.org/10.1523/JNEUROSCI.2726-11.2013CrossRefGoogle ScholarPubMed
Wang, N., Perkins, E., Zhou, L., Warren, S. & May, P.J. ( 2017 ). Reticular formation connections underlying horizontal gaze: The central mesencephalic reticular formation (cMRF) as a conduit for the collicular saccade signal. Frontiers in Neuroanatomy 11, 36. https://doi.org/10.3389/fnana.2017.00036CrossRefGoogle ScholarPubMed
Wasicky, R., Horn, A.K.E. & Büttner-Ennever, J.A. ( 2004 ). Twitch and nontwitch motoneuron subgroups in the oculomotor nucleus of monkeys receive different afferent projections. Journal of Comparative Neurology 479, 117–129. http://dx.doi.org/10.1002/cne.20296CrossRefGoogle ScholarPubMed
Weitemier, A.Z. & Ryabinin, A.E. ( 2005 ). Lesions of the Edinger–Westphal nucleus alter food and water consumption. Behavioral Neuroscience 119, 1235–1243. http://dx.doi.org/10.1037/0735-7044.119.5.1235CrossRefGoogle ScholarPubMed
Weninger, S.C., Peters, L.L. & Majzoub, J.A. ( 2000 ). Urocortin expression in the Edinger–Westphal nucleus is up-regulated by stress and corticotropin-releasing hormone deficiency. Endocrinology 141, 256–263. http://dx.doi.org/10.1210/endo.141.1.7277CrossRefGoogle ScholarPubMed
Zeeh, C., Hess, B.J. & Horn, A.K. ( 2013 ). Calretinin inputs are confined to motoneurons for upward eye movements in monkey. Journal of Comparative Neurology 521, 3154–3166. http://dx.doi.org/10.1002/cne.23337CrossRefGoogle ScholarPubMed
Zhou, L., Warren, S. & May, P.J. ( 2008 ). The feedback circuit connecting the central mesencephalic reticular formation and the superior colliculus in the macaque monkey: Tectal connections. Experimental Brain Research 189, 485–496. http://dx.doi.org/10.1007/s00221-008-1444-3CrossRefGoogle ScholarPubMed
Zuniga, A. & Ryabinin, A.E. ( 2020 ). Involvement of centrally projecting Edinger–Westphal nucleus neuropeptides in actions of addictive drugs. Brain Science 10, 67. https://doi.org/10.3390/brainsci10020067CrossRefGoogle ScholarPubMed