Hostname: page-component-cd9895bd7-jn8rn Total loading time: 0 Render date: 2024-12-25T04:34:32.101Z Has data issue: false hasContentIssue false
  • English
  • Français

Cerebellar projections to the macaque midbrain tegmentum: Possible near response connections

Published online by Cambridge University Press:  12 May 2021

Martin O. Bohlen ,
Paul D. Gamlin ,
Susan Warren  and
Paul J. May Open the ORCID record for Paul J. May [Opens in a new window]
Martin O. Bohlen
Affiliation:
Department of Biomedical Engineering, Duke University, Durham, North Carolina
Paul D. Gamlin
Affiliation:
Department of Ophthalmology and Visual Sciences, University of Alabama at Birmingham, Birmingham, Alabama
Susan Warren
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, Mississippi
Paul J. May*
Affiliation:
Department of Neurobiology and Anatomical Sciences, University of Mississippi Medical Center, Jackson, Mississippi Department of Ophthalmology, University of Mississippi Medical Center, Jackson, Mississippi Department of Neurology, University of Mississippi Medical Center, Jackson, Mississippi
*
*Corresponding author: Paul J. May, email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Since most gaze shifts are to targets that lie at a different distance from the viewer than the current target, gaze changes commonly require a change in the angle between the eyes. As part of this response, lens curvature must also be adjusted with respect to target distance by the ciliary muscle. It has been suggested that projections by the cerebellar fastigial and posterior interposed nuclei to the supraoculomotor area (SOA), which lies immediately dorsal to the oculomotor nucleus and contains near response neurons, support this behavior. However, the SOA also contains motoneurons that supply multiply innervated muscle fibers (MIFs) and the dendrites of levator palpebrae superioris motoneurons. To better determine the targets of the fastigial nucleus in the SOA, we placed an anterograde tracer into this cerebellar nucleus in Macaca fascicularis monkeys and a retrograde tracer into their contralateral medial rectus, superior rectus, and levator palpebrae muscles. We only observed close associations between anterogradely labeled boutons and the dendrites of medial rectus MIF and levator palpebrae motoneurons. However, relatively few of these associations were present, suggesting these are not the main cerebellar targets. In contrast, labeled boutons in SOA, and in the adjacent central mesencephalic reticular formation (cMRF), densely innervated a subpopulation of neurons. Based on their location, these cells may represent premotor near response neurons that supply medial rectus and preganglionic Edinger–Westphal motoneurons. We also identified lens accommodation-related cerebellar afferent neurons via retrograde trans-synaptic transport of the N2c rabies virus from the ciliary muscle. They were found bilaterally in the fastigial and posterior interposed nuclei, in a distribution which mirrored that of neurons retrogradely labeled from the SOA and cMRF. Our results suggest these cerebellar neurons coordinate elements of the near response during symmetric vergence and disjunctive saccades by targeting cMRF and SOA premotor neurons.

Keywords

vergenceoculomotorsaccadefastigialtrans-synaptic transport
Type
Research Article
Information
Visual Neuroscience , Volume 38 , 2021 , E007
Check for updates
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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

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. doi:10.3389/fnana.2015.00153.CrossRefGoogle ScholarPubMed
Angaut, P. & Bowsher, D. (1970). Ascending projections of the medial cerebellar (fastigial) nucleus: An experimental study in the cat. Brain Research 24, 49–68.CrossRefGoogle ScholarPubMed
Bando, T., Ishihara, A. & Tsukahara, N. (1979). Interpositus neurons controlling lens accommodation. Proceedings of the Japanese Academy 55, 153–156.CrossRefGoogle Scholar
Bando, T., Tsukuda, K., Yamamoto, N., Maeda, J. & Tsukahara, N. (1984). Physiological identification of midbrain neurons related to lens accommodation in cats. Journal of Neurophysiology 52, 870–878.CrossRefGoogle ScholarPubMed
Barash, S., Melikyan, A., Sivakov, A., Zhang, M., Glickstein, M. & Thier, P. (1999). Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. Journal of Neuroscience 19, 10931–10939.CrossRefGoogle ScholarPubMed
Batton, R.R. III, Jayaraman, A., Ruggiero, D. & Carpenter, M.B. (1977). Fastigial efferent projections in the monkey: An autoradiographic study. Journal of Comparative Neurology 174, 281–305.CrossRefGoogle Scholar
Becker, W. & Fuchs, A.F. (1988). Lid-eye coordination during vertical gaze changes in man and monkey. Journal of Neurophysiology 60, 1227–1252.CrossRefGoogle ScholarPubMed
Bohlen, M.O., Warren, S. & May, P.J. (2017a). A central mesencephalic reticular formation projection to medial rectus motoneurons supplying singly and multiply innervated extraocular muscle fibers. Journal of Comparative Neurology 525, 2000–2018.CrossRefGoogle Scholar
Bohlen, M.O., Warren, S., Mustari, M.J. & May, P.J. (2017b). Examination of feline extraocular motoneuron pools as a function of muscle fiber innervation type and muscle layer. Journal of Comparative Neurology 525, 919–935.CrossRefGoogle Scholar
Bour, L.J., Aramideh, M. & de Visser, B.W. (2000). Neurophysiological aspects of eye and eyelid movements during blinking in humans. Journal of Neurophysiology 83, 166–176.CrossRefGoogle ScholarPubMed
Bourrelly, C., Quinet, J. & Goffart, L. (2018). Pursuit disorder and saccade dysmetria after caudal fastigial inactivation in the monkey. Journal of Neurophysiology 120, 1640–1654. doi:10.1152/jn.00278.2018.CrossRefGoogle 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.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.CrossRefGoogle ScholarPubMed
Chaturvedi, V. & van Gisbergen, J.A. (1997). Specificity of saccadic adaptation in three-dimensional space. Vision Research 37, 1367–1382.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Chen, F.P. & Evinger, C. (2006). Cerebellar modulation of trigeminal reflex blinks: Interpositus neurons. Journal of Neuroscience 26, 10569–10576.CrossRefGoogle ScholarPubMed
Chiarandini, D.J. & Stefani, E. (1979). Electrophysiological identification of two types of fibres in rat extraocular muscles. Journal of Physiology 290, 453–465.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
Das, V.E. (2012). Responses of cells in the midbrain near-response area in monkeys with strabismus. Investigative Ophthalmology and Visual Science 53, 3858–3864.CrossRefGoogle ScholarPubMed
Dash, S. & Thier, P. (2014). Cerebellum-dependent motor learning: Lessons from adaptation of eye movements in primates. Progress in Brain Research 210, 121–155.CrossRefGoogle ScholarPubMed
Delgado-García, J.M. & Gruart, A. (2002). The role of interpositus nucleus in eyelid conditioned responses. Cerebellum 1, 289–308.CrossRefGoogle ScholarPubMed
Eberhorn, A.C., Ardeleanu, P., Büttner-Ennever, J.A. & Horn, A.K. (2005). Histochemical differences between motoneurons supplying multiply and singly innervated extraocular muscle fibers. Journal of Comparative Neurology 491, 352–366.CrossRefGoogle ScholarPubMed
Eberhorn, A.C., Büttner-Ennever, J.A. & Horn, A.K. (2006). Identification of motoneurons supplying multiply- or singly-innervated extraocular muscle fibers in the rat. Neuroscience 137, 891–903.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Erichsen, J.T., Wright, N.F. & May, P.J. (2014). Morphology and ultrastructure of medial rectus subgroup motoneurons in the macaque monkey. Journal of Comparative Neurology 522, 626–641.CrossRefGoogle ScholarPubMed
Erkelens, I.M., Bobier, W.R., Macmillan, A.C., Maione, N.L., Martin Calderon, C., Patterson, H. & Thompson, B. (2020). A differential role for the posterior cerebellum in the adaptive control of convergence eye movements. Brain Stimulation 13, 215–228.CrossRefGoogle 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
Fanardjian, V.V. & Manvelyan, L.R. (1984). Peculiarities of cerebellar excitation of facial nucleus motoneurons. Neuroscience Letters 49, 265–270.CrossRefGoogle ScholarPubMed
Fuchs, A.F., Robinson, F.R. & Straube, A. (1993). Role of the caudal fastigial in saccade generation. I. Neuronal discharge pattern. Journal of Neurophysiology 70, 1723–1740, 1993.CrossRefGoogle ScholarPubMed
Fuchs, A.F., Robinson, F.R. & Straube, A. (1994). Participation of the caudal fastigial nucleus in smooth-pursuit eye movements. I. Neuronal activity. Journal of Neurophysiology 72, 2714–2728.CrossRefGoogle ScholarPubMed
Gamlin, P.D., Zhang, Y., Clendaniel, R.A. & Mays, L.E. (1994). Behavior of identified Edinger-Westphal neurons during ocular accommodation. Journal of Neurophysiology 72, 2368–2382.CrossRefGoogle ScholarPubMed
Gamlin, P.D.R. & Zhang, H.Y. (1996). Effects of muscimol blockade of the posterior fastigial nucleus on vergence and ocular accommodation in the primate. Society for Neuroscience Abstracts 22, 2034.Google Scholar
Gardner, E.P. & Fuchs, A.F. (1975). Single-unit responses to natural vestibular stimuli and eye movements in deep cerebellar nuclei of the alert rhesus monkey. Journal of Neurophysiology 38, 627–649.CrossRefGoogle ScholarPubMed
Gonzalez-Joekes, J. & Schreurs, B.G. (2012). Anatomical characterization of a rabbit cerebellar eyeblink premotor pathway using pseudorabies and identification of a local modulatory network in anterior interpositus. Journal of Neuroscience 32, 12472–12487.CrossRefGoogle ScholarPubMed
Gonzalo-Ruiz, A. & Leichnetz, G.R. (1990). Connections of the caudal cerebellar interpositus complex in a New World monkey (Cebus apella). Brain Research Bulletin 25, 919–927.CrossRefGoogle Scholar
Gonzalo-Ruiz, A., Leichnetz, G.R. & Hardy, S.G. (1990). Projections of the medial cerebellar nucleus to oculomotor-related midbrain areas in the rat: An anterograde and retrograde HRP study. Journal of Comparative Neurology 296, 427–436.CrossRefGoogle ScholarPubMed
Gonzalo-Ruiz, A., Leichnetz, G.R. & Smith, D.J. (1988). Origin of cerebellar projections to the region of the oculomotor complex, medial pontine reticular formation, and superior colliculus in New World monkeys: A retrograde horseradish peroxidase study. Journal of Comparative Neurology 268, 508–526.CrossRefGoogle ScholarPubMed
Hepp, K., Henn, V. & Jaeger, J. (1982). Eye movement related neurons in the cerebellar nuclei of the alert monkey. Experimental Brain Research 45, 253–264.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 USA 116, 3837–3846.CrossRefGoogle ScholarPubMed
Hopp, J.J. & Fuchs, A.F. (2004). The characteristics and neuronal substrate of saccadic eye movement plasticity. Progress in Neurobiology 72, 27–53.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.CrossRefGoogle ScholarPubMed
Horn, A.K.E. & Büttner-Ennever, J.A. (2008). Brainstem circuits controlling lid-eye coordination in monkey. Progress in Brain Research 171, 87–95. doi:10.1016/S0079-123(08)00612-2.CrossRefGoogle ScholarPubMed
Hosoba, M., Bando, T. & Tsukahara, N. (1978). The cerebellar control of accommodation of the eye in the cat. Brain Research 153, 495–505.CrossRefGoogle ScholarPubMed
Iwamoto, Y. & Kaku, Y. (2010). Saccade adaptation as a model of learning in voluntary movements. Experimental Brain Research 204, 145–162. doi:10.1007/s00221-010-2314-3.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Joshi, A.C. & Das, V.E. (2013). Muscimol inactivation of caudal fastigial nucleus. Journal of Neurophysiology 110, 1882–1891.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Kawamura, S., Hattori, S., Higo, S. & Matsuyama, T. (1982). The cerebellar projections to the superior colliculus and pretectum in the cat: An autoradiographic and horseradish peroxidase study. Neuroscience 7, 1673–1689.CrossRefGoogle ScholarPubMed
Kim, G., Laurens, J., Yakusheva, T.A. & Blazquez, P.M. (2019). The macaque cerebellar flocculus outputs a forward model of eye movement. Frontiers in Integrative Neuroscience 13, 12.CrossRefGoogle ScholarPubMed
Kojima, Y., Soetedjo, R. & Fuchs, A.F. (2011). Effect of inactivation and disinhibition of the oculomotor vermis on saccade adaptation. Brain Research 1401, 30–39.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Leigh, R.J. & Zee, D.S. (2015). The Neurology of Eye Movements (5th ed.). Oxford, UK: Oxford University Press, pp. 520–568.CrossRefGoogle Scholar
Lisberger, S.G. (2010). Visual guidance of smooth-pursuit eye movements: Sensation, action, and what happens in between. Neuron 66, 477–491. doi:10.1016/j.neuron.2010.03.027.CrossRefGoogle ScholarPubMed
Lv, X., Chen, Y., Tan, W., Yu, Y., Zou, H., Shao, Y., Zan, S., Tao, J. & Miao, W. (2020). Functional neuroanatomy of the human accommodation response to an “E” target varying from −3 to −6 diopters. Frontiers in Integrative Neuroscience 14, 29.CrossRefGoogle Scholar
Maxwell, J.S. & Schor, C.M. (1994). Mechanisms of vertical phoria adaptation revealed by time-course and two-dimensional spatiotopic maps. Vision Research 34, 241–251.CrossRefGoogle ScholarPubMed
May, P.J., Baker, R.G. & Chen, B. (2002). The eyelid levator muscle: Servant of two masters. Movement Disorders 17(Suppl 2), S4–S7.CrossRefGoogle ScholarPubMed
May, P.J., Billig, I., Gamlin, P.D. & Quinet, J. (2019). Central mesencephalic reticular formation control of the near response: Lens accommodation circuits. Journal of Neurophysiology 21, 1692–1703.CrossRefGoogle Scholar
May, P.J. & Gamlin, P.D. (2020). Is primate lens accommodation unilaterally or bilaterally controlled? Investigative Ophthalmology and Visual Science 61, 5.CrossRefGoogle ScholarPubMed
May, P.J., Hartwich-Young, R., Nelson, J., Sparks, D.L. & Porter, J.D. (1990). Cerebellotectal pathways in the macaque: Implications for collicular generation of saccades. Neuroscience 36, 305–324.CrossRefGoogle ScholarPubMed
May, P.J., Porter, J.D. & Gamlin, P.D. (1992). Interconnections between the primate cerebellum and midbrain near-response regions. Journal of Comparative Neurology 315, 98–116.CrossRefGoogle 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.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
May, P.J., Warren, S., Billig, I., Quinet, J.J. & Gamlin, P.D. (2018a). A new tectal premotor input for the control of lens accommodation. Society for Neuroscience Abstracts 44, 398.07.Google Scholar
May, P.J., Warren, S., Gamlin, P.D. & Billig, I. (2018b). An anatomic characterization of the midbrain near response neurons in the macaque monkey. Investigative Ophthalmology and Visual Science 59, 1486–1502.CrossRefGoogle Scholar
Mays, L.E. (1984). Neural control of vergence eye movements: Convergence and divergence neurons in midbrain. Journal of Neurophysiology 51, 1091–1108.CrossRefGoogle ScholarPubMed
Mays, L.E., Porter, J.D., Gamlin, P.D.R. & Tello, C.A. (1986). Neural control of vergence eye movements: Neurons encoding vergence velocity. Journal of Neurophysiology 56, 1007–1021.CrossRefGoogle ScholarPubMed
McCann, B.C., Hayhoe, M.M. & Geisler, W.S. (2018). Contributions of monocular and binocular cues to distance discrimination in natural scenes. Journal of Vision 18, 1–15.CrossRefGoogle ScholarPubMed
McCrea, R.A., 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. doi:10.1002/cne.902430302.CrossRefGoogle ScholarPubMed
Milder, D.G. & Reinecke, R.D. (1983). Phoria adaptation to prisms. A cerebellar-dependent response. Archives of Neurology 40, 339–342.CrossRefGoogle ScholarPubMed
Nitta, T., Akao, T., Kurkin, S. & Fukushima, K. (2008). Involvement of the cerebellar dorsal vermis in vergence eye movements in monkeys. Cerebral Cortex 18, 1042–1057. doi:10.1093/cercor/bhm143.CrossRefGoogle ScholarPubMed
Noda, H., Sugita, S. & Ikeda, Y. (1990). Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. Journal of Comparative Neurology 302, 330–348. doi:10.1002/cne.903020211.CrossRefGoogle ScholarPubMed
Pallus, A.C., Walton, M.M.G. & Mustari, M.J. (2018a). Response of supraoculomotor area neurons during combined saccade-vergence movements. Journal of Neurophysiology 119, 585–596.CrossRefGoogle Scholar
Pallus, A., Walton, M.M.G. & Mustari, M. (2018b). Activity of near-response cells during disconjugate saccades in strabismic monkeys. Journal of Neurophysiology 120, 2282–2295.CrossRefGoogle Scholar
Paxinos, G., Huang, X-F & Toga, A.W. (2000). The Rhesus Monkey Brain in Stereotaxic Coordinates . San Diego: Academic Press.Google Scholar
Person, R.J., Andrezik, J.A., Dormer, K.J. & Foreman, R.D. (1986). Fastigial nucleus projections in the midbrain and thalamus in dogs. Neuroscience 18, 105–120.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Prevosto, V., Graf, W. & Ugolini, G. (2017). The control of eye movements by the cerebellar nuclei: Polysynaptic projections from the fastigial, interpositus posterior and dentate nuclei to lateral rectus motoneurons in primates. European Journal of Neuroscience 45, 1538–1552.CrossRefGoogle ScholarPubMed
Quinet, J. & Goffart, L. (2007). Head-unrestrained gaze shifts after muscimol injection in the caudal fastigial nucleus of the monkey. Journal of Neurophysiology 98, 3269–3283. doi:10.1152/jn.00741.2007.CrossRefGoogle ScholarPubMed
Quinet, J. & Goffart, L. (2009). Electrical microstimulation of the fastigial oculomotor region in the head-unrestrained monkey. Journal of Neurophysiology 102, 320–336. doi:10.1152/jn.90716.2008.CrossRefGoogle ScholarPubMed
Quinet, J., Schultz, K., May, P.J. & Gamlin, P.D. (2020). Neural control of rapid binocular eye movements: Saccade-vergence burst neurons. Proceedings of the National Academy of Science U S A 117, 29123–29132. doi:10.1073/pnas.2015318117.CrossRefGoogle ScholarPubMed
Raghavan, R.T. & Lisberger, S.G. (2017). Responses of Purkinje cells in the oculomotor vermis of monkeys during smooth pursuit eye movements and saccades: Comparison with floccular complex. Journal of Neurophysiology 118, 986–1001. doi:10.1152/jn.00209.2017.CrossRefGoogle ScholarPubMed
Raux, H., Iseni, F., Lafay, F. & Blondel, D. (1997). Mapping of monoclonal antibody epitopes of the rabies virus P protein. Journal of General Virology 78, 119–124.CrossRefGoogle ScholarPubMed
Richter, H.O., Costello, P., Sponheim, S.R., Lee, J.T. & Pardo, J.V. (2004). Functional neuroanatomy of the human near/far response to blur cues: Eye-lens accommodation/vergence to point targets varying in depth. European Journal of Neuroscience 20, 2722–2732.CrossRefGoogle ScholarPubMed
Richter, H.O., Lee, J.T. & Pardo, J.V. (2000). Neuroanatomical correlates of the near response: Voluntary modulation of accommodation/vergence in the human visual system. European Journal of Neuroscience 12, 311–321.CrossRefGoogle ScholarPubMed
Ruigrok, T.J., van Touw, S. & Coulon, P. (2016). Caveats in transneuronal tracing with unmodified rabies virus: An evaluation of aberrant results using a nearly perfect tracing technique. Frontiers in Neural Circuits 10, 46.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Sánchez-Campusano, R., Gruart, A., Fernández-Mas, R. & Delgado-Garcia, J.M. (2012). An agonist-antagonist cerebellar nuclear system controlling eyelid kinematics during motor learning. Frontiers in Neuroanatomy 6, 8.CrossRefGoogle ScholarPubMed
Sander, T., Sprenger, A., Neumann, G., Machner, B., Gottschalk, S., Rambold, H. & Helmchen, C. (2009). Vergence deficits in patients with cerebellar lesions. Brain 132, 103–115.CrossRefGoogle ScholarPubMed
Schor, C.M., Maxwell, J.S., McCandless, J. & Graf, E. (2002). Adaptive control of vergence in humans. Annals of the New York Academy of Science 956, 297–305.CrossRefGoogle ScholarPubMed
Schor, C.M. & McCandless, J.W. (1995). An adaptable association between vertical and horizontal vergence. Vision Research 35, 3519–3527.CrossRefGoogle ScholarPubMed
Soetedjo, R., Kojima, Y. & Fuchs, A.F. (2008). Complex spike activity in the oculomotor vermis of the cerebellum: A vectorial error signal for saccade motor learning? Journal of Neurophysiology 100, 1949–1966.CrossRefGoogle ScholarPubMed
Soetedjo, R., Kojima, Y. & Fuchs, A.F. (2019). How cerebellar motor learning keeps saccades accurate. Journal of Neurophysiology 121, 2153–2162. doi:10.1152/jn.00781.2018.CrossRefGoogle ScholarPubMed
Spencer, R.F. & Porter, J.D. (2006). Biological organization of the extraocular muscles. In Neuroanatomy of the Oculomotor System, Ed. Büttner-Ennever, J.A. Progress in Brain Research 151, 43–80.CrossRefGoogle Scholar
Stanton, G.B. (1980). Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: An anterograde degeneration study. Journal of Comparative Neurology 190, 699–731.CrossRefGoogle Scholar
Sun, L.W. (2012). Transsynaptic tracing of conditioned eyeblink circuits in the mouse cerebellum. Neuroscience 203, 122–134.CrossRefGoogle ScholarPubMed
Szabo, J. & Cowan, W.M. (1984). A stereotaxic atlas of the brain of the cynomologous monkey (Macaca fascicularis). Journal of Comparative Neurology 222, 265–300.CrossRefGoogle Scholar
Takagi, M., Tamargo, R. & Zee, D.S. (2003). Effects of lesions of the cerebellar oculomotor vermis on eye movements in primate: Binocular control. Progress in Brain Research 142, 19–33. doi:10.1016/S0079-6123(03)42004-9.CrossRefGoogle ScholarPubMed
Takagi, M., Zee, D.S. & Tamargo, R.J. (2000). Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: Smooth pursuit. Journal of Neurophysiology 83, 2047–2062.CrossRefGoogle ScholarPubMed
Takeichi, N., Kaneko, C.R.S. & Fuchs, A.F. (2007). Activity changes in monkey superior colliculus during saccade adaptation. Journal of Neurophysiology 97, 4096–4107. doi:10.1152/jn.01278.2006.CrossRefGoogle ScholarPubMed
Tang, X., Büttner-Ennever, J.A., Mustari, M.J. & Horn, A.K.E. (2015). Internal organization of medial rectus and inferior rectus muscle neurons in the C group of the oculomotor nucleus in monkey. Journal of Comparative Neurology 523, 1809–1823.CrossRefGoogle Scholar
Waitzman, D.M., Van Horn, M.R. & Cullen, K.E. (2008). Neuronal evidence for individual eye control in the primate cMRF. Progress in Brain Research 171, 143–150.CrossRefGoogle ScholarPubMed
Walton, M.M.G., Pallus, A. & Mustari, M. (2019). A rhesus monkey with a naturally occurring impairment of disparity vergence. II. Abnormal near response cell activity in the supraoculomotor area. Investigative Ophthalmology and Visual Science 60, 1670–1676.CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Weitemier, A.Z. & Ryabinin, A.E. (2006). Urocortin 1 in the dorsal raphe regulates food and fluid consumption, but not ethanol preference in C57BL/6J mice. Neuroscience 137, 1439–1445.CrossRefGoogle Scholar
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. doi:10.1002/cne.23337.CrossRefGoogle ScholarPubMed
Zhang, H. & Gamlin, P.D. (1996). Single-unit activity within the posterior fastigial nucleus during vergence and accommodation in the alert primate. Society for Neuroscience Abstracts 22, 2034 #801.1.Google Scholar
Zhang, H. & Gamlin, P.D. (1998). Neurons in the posterior interposed nucleus of the cerebellum related to vergence and accommodation. I. Steady-state characteristics. Journal of Neurophysiology 79, 1255–1269.CrossRefGoogle ScholarPubMed
Zhang, Y., Mays, L.E. & Gamlin, P.D. (1992). Characteristics of near response cells projecting to the oculomotor nucleus. Journal of Neurophysiology 67, 944–960.CrossRefGoogle ScholarPubMed