1932

Abstract

Eye movements are indispensable for visual image stabilization during self-generated and passive head and body motion and for visual orientation. Eye muscles and neuronal control elements are evolutionarily conserved, with novel behavioral repertoires emerging during the evolution of frontal eyes and foveae. The precise execution of eye movements with different dynamics is ensured by morphologically diverse yet complementary sets of extraocular muscle fibers and associated motoneurons. Singly and multiply innervated muscle fibers are controlled by motoneuronal subpopulations with largely selective premotor inputs from task-specific ocular motor control centers. The morphological duality of the neuromuscular interface is matched by complementary biochemical and molecular features that collectively assign different physiological properties to the motor entities. In contrast, the functionality represents a continuum where most motor elements contribute to any type of eye movement, although within preferential dynamic ranges, suggesting that signal transmission and muscle contractions occur within bands of frequency-selective pathways.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-vision-100119-125043
2021-09-15
2024-12-13
Loading full text...

Full text loading...

/deliver/fulltext/vision/7/1/annurev-vision-100119-125043.html?itemId=/content/journals/10.1146/annurev-vision-100119-125043&mimeType=html&fmt=ahah

Literature Cited

  1. Ahlfeld J, Mustari M, Horn AKE. 2011. Sources of calretinin inputs to motoneurons of extraocular muscles involved in upgaze. Ann. N. Y. Acad. Sci. 1233:91–99
    [Google Scholar]
  2. Ahmadi M, Liu J-X, Brännström T, Andersen PM, Stål P, Pedrosa-Domellöf F. 2010. Human extraocular muscles in ALS. Investig. Ophthalmol. Vis. Sci. 51:3494–501
    [Google Scholar]
  3. Baker R, Evinger C, McCrea RA. 1981. Some thoughts about the three neurons in the vestibular ocular reflex. Ann. N. Y. Acad. Sci. 374:171–88
    [Google Scholar]
  4. Baryshnikova LM, Croes SA, von Bartheld CS 2007. Classification and development of myofiber types in the superior oblique extraocular muscle of chicken. Anat. Rec. 290:1526–41
    [Google Scholar]
  5. Benítez-Temiño B, Davis-López de Carrizosa MA, Morcuende S, Matarredona ER, de la Cruz RR, Pastor AM 2016. Functional diversity of neurotrophin actions on the oculomotor system. Int. J. Mol. Sci. 17:2016
    [Google Scholar]
  6. Bianco IH, Kampff AR, Engert F. 2011. Prey capture behavior evoked by simple visual stimuli in larval zebrafish. Front. Syst. Neurosci. 5:101
    [Google Scholar]
  7. Blumer R, Maurer-Gesek B, Gesslbauer B, Blumer M, Pechriggl E et al. 2016. Palisade endings are a constant feature in the extraocular muscles of frontal-eyed, but not lateral-eyed, animals. Investig. Ophthalmol. Vis. Sci. 57:320–31
    [Google Scholar]
  8. Blumer R, Streicher J, Davis-López de Carrizosa MA, de la Cruz RR, Pastor AM 2017. Palisade endings of extraocular muscles develop postnatally following different time courses. Investig. Ophthalmol. Vis. Sci. 58:5105–21
    [Google Scholar]
  9. Bohlen MO, Bui K, Stahl JS, May PJ, Warren S 2019. Mouse extraocular muscles and the musculotopic organization of their innervation. Anat. Rec. 302:1865–85
    [Google Scholar]
  10. Bohlen MO, Warren S, May PJ. 2017a. A central mesencephalic reticular formation projection to medial rectus motoneurons supplying singly and multiply innervated extraocular muscle fibers. J. Comp. Neurol. 525:2000–18
    [Google Scholar]
  11. Bohlen MO, Warren S, Mustari MJ, May PJ 2017b. Examination of feline extraocular motoneuron pools as a function of muscle fiber innervation type and muscle layer. . J. Comp. Neurol. 525:919–35
    [Google Scholar]
  12. Branoner F, Chagnaud BP, Straka H. 2016. Ontogenetic development of vestibulo-ocular reflexes in amphibians. Front. Neural Circuits 10:91
    [Google Scholar]
  13. Briggs MM, Schachat F. 2002. The superfast extraocular myosin (MYH13) is localized to the innervation zone in both the global and orbital layers of rabbit extraocular muscle. J. Exp. Biol. 205:3133–42
    [Google Scholar]
  14. Brini M, Calì T, Ottolini D, Carafoli E. 2014. Neuronal calcium signaling: function and dysfunction. Cell Mol. Life Sci. 71:2787–814
    [Google Scholar]
  15. Brockington A, Ning K, Heath P, Wood E, Kirby J et al. 2013. Unravelling the enigma of selective vulnerability in neurodegeneration: Motor neurons resistant to degeneration in ALS show distinct gene expression characteristics and decreased susceptibility to excitotoxicity. Acta Neuropathol 125:95–109
    [Google Scholar]
  16. Brueckner JK, Ashby LP, Prichard JR, Porter JD. 1999. Vestibulo-ocular pathways modulate extraocular muscle myosin expression patterns. Cell Tiss. Res. 295:477–84
    [Google Scholar]
  17. Brueckner JK, Porter JD. 1998. Visual system maldevelopment disrupts extraocular muscle-specific myosin expression. J. Appl. Physiol. 85:584–92
    [Google Scholar]
  18. Budak MT, Bogdanovich S, Wiesen MHJ, Lozynska O, Khurana TS, Rubinstein NA. 2004. Layer-specific differences of gene expression in extraocular muscles identified by laser-capture microscopy. Physiol. Genom. 20:55–65
    [Google Scholar]
  19. Büttner U, Büttner-Ennever JA. 2006. Present concepts of oculomotor organization. Prog. Brain Res. 151:1–42
    [Google Scholar]
  20. Büttner-Ennever JA. 2006. The extraocular motor nuclei: organization and functional neuroanatomy. Prog. Brain Res. 151:95–125
    [Google Scholar]
  21. Büttner-Ennever JA, Akert K. 1981. Medial rectus subgroups of the oculomotor nucleus and their abducens internuclear input in the monkey. J. Comp. Neurol. 197:17–27
    [Google Scholar]
  22. Büttner-Ennever JA, Cohen B, Horn AKE, Reisine H. 1996. Pretectal projections to the oculomotor complex of the monkey and their role in eye movements. J. Comp. Neurol. 366:348–59
    [Google Scholar]
  23. Büttner-Ennever JA, Horn AKE. 1996. Pathways from cell groups of the paramedian tracts to the floccular region. Ann. N. Y. Acad. Sci. 781:532–40
    [Google Scholar]
  24. Büttner-Ennever JA, Horn AKE. 2002. The neuroanatomical basis of oculomotor disorders: the dual motor control of extraocular muscles and its possible role in proprioception. Curr. Opin. Neurol. 15:35–43
    [Google Scholar]
  25. Büttner-Ennever JA, Horn AKE, Scherberger H, D'Ascanio P. 2001. Motoneurons of twitch and non-twitch extraocular muscle fibers in the abducens, trochlear, and oculomotor nuclei of monkeys. . J. Comp. Neurol. 438:318–35
    [Google Scholar]
  26. Büttner-Ennever JA, Konakci KZ, Blumer R. 2006. Sensory control of extraocular muscles. Prog. Brain Res. 151:81–93
    [Google Scholar]
  27. Cabrera B, Portillo F, Pasaro R, Delgado-García JM. 1988. Location of motoneurons and internuclear neurons within the rat abducens nucleus by means of horseradish peroxidase and fluorescent double labeling. Neurosci. Lett. 87:1–6
    [Google Scholar]
  28. Cabrera B, Torres B, Pásaro R, Pastor AM, Delgado-García JM. 1992. A morphological study of abducens nucleus motoneurons and internuclear neurons in the goldfish (Carassius auratus). Brain Res. Bull. 28:137–44
    [Google Scholar]
  29. Carrascal L, Nieto-Gonzalez JL, Cameron WE, Torres B, Nunez-Abades PA. 2005. Changes during the postnatal development in physiological and anatomical characteristics of rat motoneurons studied in vitro. Brain Res. Rev. 49:377–87
    [Google Scholar]
  30. Carrascal L, Nieto-Gonzales JL, Nuñez-Abades P, Torres B. 2006. Temporal sequence of changes in electrophysiological properties of oculomotor motoneurons during postnatal development. Neuroscience 140:1223–37
    [Google Scholar]
  31. Carrascal L, Nieto-Gonzalez JL, Torres B, Nunez-Abades P. 2009. Changes in somatodendritic morphometry of rat oculomotor nucleus motoneurons during postnatal development. J. Comp. Neurol. 514:189–202
    [Google Scholar]
  32. Cetin H, Beeson D, Vincent A, Webster R. 2020. The structure, function, and physiology of the fetal and adult acetylcholine receptor in muscle. Front. Mol. Neurosci. 13:581097
    [Google Scholar]
  33. Chamma I, Chevy Q, Poncer JC, Lévi S. 2012. Role of the neuronal K-Cl co-transporter KCC2 in inhibitory and excitatory neurotransmission. Front. Cell. Neurosci. 6:5
    [Google Scholar]
  34. Che Ngwa E, Zeeh C, Messoudi A, Büttner-Ennever JA, Horn AKE 2014. Delineation of motoneuron subgroups supplying individual eye muscles in the human oculomotor nucleus. Front. Neuroanat. 8:2
    [Google Scholar]
  35. Chen J, von Bartheld CS 2004. Role of exogenous and endogenous trophic factors in the regulation of extraocular muscle strength during development. Investig. Ophthalmol. Vis. Sci. 45:3538–45
    [Google Scholar]
  36. Chiarandini DJ, Stefani E 1979. Electrophysiological identification of two types of fibres in rat extraocular muscles. J. Physiol. 290:453–65
    [Google Scholar]
  37. Clendaniel RA, Mays LE. 1994. Characteristics of antidromically identified oculomotor internuclear neurons during vergence and versional eye movements. J. Neurophysiol. 71:1111–27
    [Google Scholar]
  38. Cochran SL, Dieringer N, Precht W. 1984. Basic optokinetic-ocular reflex pathways in the frog. J. Neurosci. 4:43–57
    [Google Scholar]
  39. Collewijn H. 1989. The vestibulo-ocular reflex: an outdated concept?. Prog. Brain Res. 80:197–209
    [Google Scholar]
  40. Colombo MN, Francolini M. 2019. Glutamate at the vertebrate neuromuscular junction: from modulation to neurotransmission. Cells 8:996
    [Google Scholar]
  41. Comley LH, Nijssen J, Frost-Nylen J, Hedlund E. 2016. Cross-disease comparison of amyotrophic lateral sclerosis and spinal muscular atrophy reveals conservation of selective vulnerability but differential neuromuscular junction pathology. J. Comp. Neurol. 524:1424–42
    [Google Scholar]
  42. Cox PG, Jeffery N 2008. Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids and modern humans. J. Anat. 213:583–96
    [Google Scholar]
  43. Croes SA, von Bartheld CS 2005. Development of the neuromuscular junction in extraocular muscles of white Leghorn chicks. Anat. Rec. 282:110–19
    [Google Scholar]
  44. Cullen KE. 2019. Vestibular processing during natural self-motion: implications for perception and action. Nat. Rev. Neurosci. 20:346–63
    [Google Scholar]
  45. Davis-López de Carrizosa MA, Morado-Díaz CJ, Miller JM, de la Cruz RR, Pastor AM 2011. Dual encoding of muscle tension and eye position by abducens motoneurons. J. Neurosci. 31:2271–79
    [Google Scholar]
  46. Davis-López de Carrizosa MA, Morado-Díaz CJ, Tena JJ, Benítez-Temiño B, Pecero ML et al. 2009. Complementary actions of BDNF and neurotrophin-3 on the firing patterns and synaptic composition of motoneurons. J. Neurosci. 29:575–87
    [Google Scholar]
  47. de la Cruz RR, Escudero M, Delgado-García JM. 1989. Behaviour of medial rectus motoneurons in the alert cat. Eur. J. Neurosci. 1:288–95
    [Google Scholar]
  48. de la Cruz RR, Pastor AM, Martínez-Guijarro FJ, López-García C, Delgado-García JM. 1992. Role of GABA in the extraocular motor nuclei of the cat: a postembedding immunocytochemical study. Neuroscience 51:911–29
    [Google Scholar]
  49. de la Cruz RR, Pastor AM, Martínez-Guijarro FJ, López-García C, Delgado-García JM. 1998. Localization of parvalbumin, calretinin, and calbindin D-28k in identified extraocular motoneurons and internuclear neurons of the cat. J. Comp. Neurol. 390:377–91
    [Google Scholar]
  50. Dean P. 1996. Motor unit recruitment in a distribution model of extraocular muscle. J. Neurophysiol. 76:727–42
    [Google Scholar]
  51. Dean P. 1997. Simulated recruitment of medial rectus motoneurons by abducens internuclear neurons: synaptic specificity versus intrinsic motoneuron properties. J. Neurophysiol. 78:1531–49
    [Google Scholar]
  52. Delgado-García JM, Del Pozo F, Baker R. 1986. Behavior of neurons in the abducens nucleus of the alert cat. I. Motoneurons. Neuroscience 17:929–52
    [Google Scholar]
  53. Delgado-García JM, Yajeya J, de Dios Navarro-López J 2006. A cholinergic mechanism underlies persistent neural activity necessary for eye fixation. Prog. Brain Res. 154:211–24
    [Google Scholar]
  54. Demer JL, Miller JM, Poukens V. 1995. Evidence for fibromuscular pulleys of the recti extraocular muscles. Investig. Ophthalmol. Vis. Sci. 36:1125–36
    [Google Scholar]
  55. Demer JL, Yeul Oh S, Poukens V 2000. Evidence for active control of rectus extrocular muscle pulleys. Investig. Ophthalmol. Vis. Sci. 41:1280–90
    [Google Scholar]
  56. Dennhag N, Liu JX, Nord H, von Hofsten J, Pedrosa Domellöf F 2020. Absence of desmin in myofibers of the zebrafish extraocular muscles. Transl. Vis. Sci. Technol. 9:1
    [Google Scholar]
  57. Dieringer N, Precht W. 1986. Functional organization of eye velocity and eye position signals in abducens motoneurons of the frog. J. Comp. Physiol. 158:179–94
    [Google Scholar]
  58. Dietrich H, Glasauer S, Straka H. 2017. Functional organization of vestibulo-ocular responses in abducens motoneurons. J. Neurosci. 37:4032–45
    [Google Scholar]
  59. Dimitrova DM, Allman BL, Shall MS, Goldberg SJ. 2009. Polyneuronal innervation of single muscle fibers in cat eye muscle: inferior oblique. J. Neurophysiol. 101:2815–21
    [Google Scholar]
  60. Donaldson IML. 2000. The functions of the proprioceptors of the eye muscles. Phil. Trans. R. Soc. Lond. B 355:1685–754
    [Google Scholar]
  61. Durand J. 1991. NMDA actions on rat abducens motoneurons. Eur. J. Neurosci. 3:621–33
    [Google Scholar]
  62. Eberhorn AC, Ardelenanu P, Büttner-Ennever JA, Horn AKE. 2005. Histochemical differences between motoneurons supplying multiply and singly innervated extraocular muscle fibers. J. Comp. Neurol. 491:352–66
    [Google Scholar]
  63. Eberhorn AC, Büttner-Ennever JA, Horn AKE. 2006. Identification of motoneurons supplying multiply- or singly-innervated extraocular muscle fibers in the rat. Neuroscience 137:891–903
    [Google Scholar]
  64. Enoka RM. 1995. Morphological features and activation patterns of motor units. J. Clin. Neurophysiol. 12:538–59
    [Google Scholar]
  65. Erichsen JT, Hodos W, Evinger C 2000. The pupillary light reflex, accommodation and convergence: comparative considerations. Accommodation and Vergence Mechanisms in the Visual System O Franzén, H Richter, L Stark 31–42 Basel: Birkhäuser
    [Google Scholar]
  66. Erichsen JT, Wright NF, May PJ. 2014. Morphology and ultrastructure of medial rectus subgroup motoneurons in the macaque monkey. J. Comp. Neurol. 522:626–41
    [Google Scholar]
  67. Evinger C. 1988. Extraocular motor nuclei: location, morphology and afferents. Rev. Oculomot. Res. 2:81–117
    [Google Scholar]
  68. Evinger C, Baker R 1991. Are there subdivisions of extraocular motoneuronal pools that can be controlled separately?. Motor Control: Concepts and Issues, ed. DR Humphrey, H-J Freund 23–31 Hoboken, NJ: Wiley
    [Google Scholar]
  69. Evinger C, Graf WM, Baker R. 1987. Extra- and intracellular HRP analysis of the organization of extraocular motoneurons and internuclear neurons in the guinea pig and rabbit. J. Comp. Neurol. 262:429–45
    [Google Scholar]
  70. Ezure K, Graf WM. 1984. A quantitative analysis of the spatial organization of the vestibulo-ocular reflexes in lateral- and frontal-eyed animals. I. Orientation of semicircular canals and extraocular muscles. Neuroscience 12:85–93
    [Google Scholar]
  71. Fairless R, Williams SK, Diem R. 2019. Calcium-binding proteins as determinants of central nervous system neuronal vulnerability to disease. Int. J. Mol. Sci. 20:2146
    [Google Scholar]
  72. Fraterman S, Khurana TS, Rubinstein NA. 2006. Identification of acetylcholine receptor subunits differentially expressed in singly and multiply innervated fibers of extraocular muscles. Investig. Ophthalmol. Vis. Sci. 47:3828–34
    [Google Scholar]
  73. Fremeau RT Jr., Troyer MD, Pahner I, Nygaard GO, Tran CH et al. 2001. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247–60
    [Google Scholar]
  74. Fritzsch B. 1998. Evolution of the vestibulo-ocular system. Otolaryngol. Head Neck Surg. 119:182–92
    [Google Scholar]
  75. Fritzsch B, Sonntag R, Dubuc R, Ohta Y, Grillner S. 1990. Organization of the six motor nuclei innervating the ocular muscles in lamprey. J. Comp. Neurol. 294:491–506
    [Google Scholar]
  76. Fuchs AF, Scudder CA, Kaneko CR. 1988. Discharge patterns and recruitment order of identified motoneurons and internuclear neurons in the monkey abducens nucleus. J. Neurophysiol. 60:1874–95
    [Google Scholar]
  77. Fukushima K, Kaneko CR. 1995. Vestibular integrators in the oculomotor system. Neurosci. Res. 22:249–58
    [Google Scholar]
  78. Gilland E, Baker R. 2005. Evolutionary patterns of cranial nerve efferent nuclei in vertebrates. Brain Behav. Evol. 66:234–54
    [Google Scholar]
  79. Gilland E, Straka H, Wong TW, Baker R, Zottoli SJ. 2014. A hindbrain segmental scaffold specifying neuronal location in the adult goldfish, Carassius auratus. J. Comp. Neurol. 522:2446–64
    [Google Scholar]
  80. Graf W, Brunken WJ. 1984. Elasmobranch oculomotor organization: anatomical and theoretical aspects of the phylogenetic development of vestibulo-oculomotor connectivity. J. Comp. Neurol. 227:569–81
    [Google Scholar]
  81. Graf W, Simpson JI. 1981. The relations between the semicircular canals, the optic axis, and the extraocular muscles in lateral-eyed and frontal-eyed animals. Prog. Oculomot. Res. 12:411–20
    [Google Scholar]
  82. Grantyn R, Grantyn A. 1978. Morphological and electrophysiological properties of cat abducens motoneurons. Exp. Brain Res. 31:249–74
    [Google Scholar]
  83. Gray TS, McMaster SE, Harvey JA, Gormezano I. 1981. Localization of retractor bulbi motoneurons in the rabbit. Brain Res 226:93–106
    [Google Scholar]
  84. Grosskreutz J, Van Den Bosch L, Keller BU 2010. Calcium dysregulation in amyotrophic lateral sclerosis. Cell Calcium 47:165–74
    [Google Scholar]
  85. Gu Y, Servello D, Han Z, Lalchandani RR, Ding JB et al. 2018. Balanced activity between Kv3 and Nav channels determines fast-spiking in mammalian central neurons. iScience 9:120–37
    [Google Scholar]
  86. Guéritaud JP. 1988. Electrical activity of rat ocular motoneurons recorded in vitro. Neuroscience 24:837–52
    [Google Scholar]
  87. Guéritaud JP, Horcholle-Bossavit G, Jami L, Thiesson D, Tyc-Dumont S 1985. Resistance to glycogen depletion of motor units in the cat rectus lateralis muscle. Exp. Brain Res. 60:542–50
    [Google Scholar]
  88. Hanson J, Lennerstrand G, Nichols KC. 1980. The postnatal development of the inferior oblique muscle of the cat. III. Fiber sizes and histochemical properties. Acta Physiol. Scand. 108:61–71
    [Google Scholar]
  89. Heath PR, Shaw PJ. 2002. Update on the glutamatergic neurotransmitter system and the role of excitotoxicity in amyotrophic lateral sclerosis. Muscle Nerve 26:438–58
    [Google Scholar]
  90. Helmchen C, Rambold H, Fuhry L, Büttner U. 1998. Deficits in vertical and torsional eye movements after uni- and bilateral muscimol inactivation of the interstitial nucleus of Cajal of the alert monkey. Exp. Brain Res. 119:436–52
    [Google Scholar]
  91. Henneman E, Somjen G, Carpenter DO. 1965. Excitability and inhibitibility of motoneurons of different sizes. J. Neurophysiol 28:599–620
    [Google Scholar]
  92. Hernández GR, Blumer R, de la Cruz RR, Pastor AM. 2019. Functional diversity of motoneurons in the oculomotor system. PNAS 116:3837–46
    [Google Scholar]
  93. Highstein SM, Holstein GR. 2006. The anatomy of the vestibular nuclei. Prog. Brain Res. 151:157–203
    [Google Scholar]
  94. Highstein SM, Karabelas A, Baker R, McCrea RA. 1982. Comparison of the morphology of physiologically identified abducens motor and internuclear neurons in the cat: a light microscopic study employing the intracellular injection of horseradish peroxidase. J. Comp. Neurol. 208:369–81
    [Google Scholar]
  95. Hoh JFY. 2021. Myosin heavy chains in extraocular muscle fibres: distribution, regulation and function. Acta Physiol. 231:e13535
    [Google Scholar]
  96. Horn AKE. 2006. The reticular formation. Prog. Brain Res 151:127–55
    [Google Scholar]
  97. Horn AKE, Helmchen C, Wahle P. 2003. GABAergic neurons in the rostral mesencephalon of the Macaque monkey that control vertical eye movements. Ann. N. Y. Acad. Sci. 1004:19–28
    [Google Scholar]
  98. Horn AKE, Horng A, Buresch N, Messoudi A, Härtig W. 2018. Identification of functional cell groups in the abducens nucleus of monkey and human by perineuronal nets and choline acetyltransferase immunolabeling. Front. Neuroanat. 12:45
    [Google Scholar]
  99. Horn AKE, Leigh RJ. 2011. The anatomy and physiology of the ocular motor system. Handb. Clin. Neurol. 102:21–69
    [Google Scholar]
  100. Ince P, Stout N, Shaw P, Slade J, Hunziker W et al. 1993. Parvalbumin and calbindin D-28k in the human motor system and in motor neuron disease. Neuropathol. Appl. Neurobiol. 19:291–99
    [Google Scholar]
  101. Isomura G. 1981. Comparative anatomy of the extrinsic ocular muscles in vertebrates. Anat. Anz. 150:498–515
    [Google Scholar]
  102. Jacoby J, Chiarandini DJ, Stefani E 1989. Electrical properties and innervation of fibers in the orbital layer of rat extraocular muscles. J. Neurophysiol. 61:116–25
    [Google Scholar]
  103. Jones MS, Ariel M 2008. Morphology, intrinsic membrane properties, and rotation-evoked responses of trochlear motoneurons in the turtle. J. Neurophysiol. 99:1187–200
    [Google Scholar]
  104. Kanning KC, Kaplan A, Henderson CE. 2010. Motor neuron diversity in development and disease. Annu. Rev. Neurosci. 33:409–40
    [Google Scholar]
  105. Ketterer C, Zeiger U, Budak MT, Rubinstein NA, Khurana TS. 2010. Identification of the neuromuscular junction transcriptome of extraocular muscle by laser capture microdissection. Investig. Ophthalmol. Vis. Sci. 51:4589–99
    [Google Scholar]
  106. Khanna S, Porter JD. 2001. Evidence for rectus extraocular muscle pulleys in rodents. Investig. Ophthalmol. Vis. Sci. 42:1986–92
    [Google Scholar]
  107. Khanna S, Richmonds C, Kaminski H, Porter JD. 2003. Molecular organization of the extraocular muscle neuromuscular junction: partial conservation of and divergence from the skeletal muscle prototype. Investig. Ophthalmol. Vis. Sci. 44:1918–26
    [Google Scholar]
  108. Kjellgren D, Thornell L-E, Andersen J, Pedrosa-Domellöf F. 2003. Myosin heavy chain isoforms in human extraocular muscles. Investig. Ophthalmol. Vis. Sci. 44:1419–25
    [Google Scholar]
  109. Krauzlis RJ, Goffart L, Hafed ZM. 2017. Neuronal control of fixation and fixational eye movements. Philos. Trans. R. Soc. Lond. B 372:20160205
    [Google Scholar]
  110. Labandeira-Garcia JL, Guerra-Seijas MJ, Labandeira-Garcia JA. 1989. The abducens motor and internuclear neurons in the rabbit: retrograde horseradish peroxidase and double fluorescent labeling. Brain Res 497:305–14
    [Google Scholar]
  111. Labandeira-Garcia JL, Guerra-Seijas MJ, Segade LA, Suarez-Nunez JM. 1987. Identification of abducens motoneurons, accessory abducens motoneurons, and abducens internuclear neurons in the chick by retrograde transport of horseradish peroxidase. J. Comp. Neurol. 259:140–49
    [Google Scholar]
  112. Lahjouji F, Barbe A, Chazal G, Bras H. 1996. Evidence for colocalization of GABA and glycine in afferents to retrogradely labelled rat abducens motoneurones. Neurosci. Lett. 206:161–64
    [Google Scholar]
  113. Lambert FM, Cardoit L, Courty E, Bougerol M, Thoby-Brisson M et al. 2018. Functional limb muscle innervation prior to cholinergic transmitter specification during early metamorphosis in Xenopus. eLife 7:e30693
    [Google Scholar]
  114. Lambert FM, Combes D, Simmers J, Straka H. 2012. Gaze stabilization by efference copy signaling without sensory feedback during vertebrate locomotion. Curr. Biol. 22:1649–58
    [Google Scholar]
  115. Land M. 2015. Eye movements of vertebrates and their relation to eye form and function. J. Comp. Physiol. 201:195–214
    [Google Scholar]
  116. Langer TP, Kaneko CR, Scudder CA, Fuchs AF. 1986. Afferents to the abducens nucleus in the monkey and cat. J. Comp. Neurol. 245:379–400
    [Google Scholar]
  117. Laslo P, Lipski J, Nicholson LF, Miles GB, Funk GD. 2001. GluR2 AMPA receptor subunit expression in motoneurons at low and high risk for degeneration in amyotrophic lateral sclerosis. Exp. Neurol. 169:461–71
    [Google Scholar]
  118. Le Masson G, Przedborski S, Abbott LF 2014. A computational model of motor neuron degeneration. Neuron 83:975–88
    [Google Scholar]
  119. Lienbacher K, Horn AE. 2012. Palisade endings and proprioception in extraocular muscles: a comparison with skeletal muscles. Biol. Cybern. 106:643–55
    [Google Scholar]
  120. Lienbacher K, Mustari M, Ying HS, Büttner-Ennever JA, Horn AKE. 2011. Do palisade endings in extraocular muscles arise from neurons in the motor nuclei?. Investig. Ophthalmol. Vis. Sci. 52:2510–19
    [Google Scholar]
  121. Lienbacher K, Ono S, Fleuriet J, Mustari M, Horn AKE. 2018. A subset of palisade endings only in the medial and inferior rectus muscle in monkey contain calretinin. Investig. Ophthalmol. Vis. Sci. 59:2944–54
    [Google Scholar]
  122. Lisberger SG. 2010. Visual guidance of smooth pursuit eye movements: sensation, action, and what happens in between. Neuron 66:477–91
    [Google Scholar]
  123. Lisberger SG, Miles FA, Optican LM. 1983. Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex. ? J. Neurosci. 3:1234–44
    [Google Scholar]
  124. Lorenzo L-E, Barbe A, Portalier P, Fritschy JM, Bras H. 2006. Differential expression of GABAA and glycine receptors in ALS-resistant versus ALS-vulnerable motoneurons: possible implications for selective vulnerability of motoneurons. Eur. J. Neurosci. 23:3161–70
    [Google Scholar]
  125. Lorenzo L-E, Russier M, Barbe A, Fritschy JM, Bras H. 2007. Differential organization of g-aminobutric acid type A and glycine receptors in the somatic and dentritic compartments of rat abducens motoneurons. J. Comp. Neurol. 504:112–216
    [Google Scholar]
  126. Lucas CA, Rhee HSM, Hoh JFY. 2018. Changes in myosin heavy chain isoforms along the length of orbital fibers in rabbit extraocular muscle. Investig. Ophthalmol. Vis. Sci. 59:1178–90
    [Google Scholar]
  127. Maciewicz RJ, Kaneko CR, Highstein SM, Baker R. 1975. Morphophysiological identification of interneurons in the oculomotor nucleus that project to the abducens nucleus in the cat. Brain Res 96:60–65
    [Google Scholar]
  128. Maier A, DeSantis M, Eldred E. 1974. The occurrence of muscle spindles in extraocular muscles of various vertebrates. J. Morphol. 143:397–408
    [Google Scholar]
  129. Matesz C, Székely G. 1977. The dorsomedial nuclear group of cranial nerves in the frog. Acta Biol. Acad. Sci. Hung. 28:461–74
    [Google Scholar]
  130. Mayadali ÜS, Fleuriet J, Mustari M, Straka H, Horn AKE 2021. Transmitter and ion channel profiles of neurons in the primate abducens and trochlear nuclei. Brain Struct. Funct 226:2125–51
    [Google Scholar]
  131. Mays LE, Gamlin PDR. 1995. Neuronal circuitry controlling the near response. Curr. Opin. Neurobiol. 5:763–68
    [Google Scholar]
  132. McClung JR, Shall MS, Goldberg J. 2001. Motoneurons of the lateral and medial rectus extrocular muscles in squirrel monkey and cat. Cell Tiss. Org. 168:220–27
    [Google Scholar]
  133. McCrea RA, Horn AKE. 2006. Nucleus prepositus. Prog. Brain Res. 151:205–30
    [Google Scholar]
  134. McCrea RA, Strassman A, Highstein SM. 1986. Morphology and physiology of abducens motoneurons and internuclear neurons intracellulary injected with horseradish peroxidase in alert squirrel monkey. J. Comp. Neurol. 243:291–308
    [Google Scholar]
  135. McCrea RA, Strassman A, Highstein SM. 1987. Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflex of the squirrel monkey. J. Comp. Neurol. 264:571–94
    [Google Scholar]
  136. McLoon LK, Christiansen SP. 2003. Increasing extraocular muscle strength with insulin-like growth factor II. Investig. Ophthalmol. Vis. Sci. 44:3866–72
    [Google Scholar]
  137. McLoon LK, Park HN, Kim J-H, Pedrosa-Domellöf F, Thompson LV. 2011. A continuum of myofibers in adult rabbit extraocular muscle: force, shortening velocity, and patterns of myosin heavy chain colocalization. J. Appl. Physiol. 111:1178–89
    [Google Scholar]
  138. McLoon LK, Rowe J, Wirtschafter JD, McCormick KM. 2004. Continuous myofiber remodeling in uninjured extraocular myofibers: myonuclear turnover and evidence for apoptosis. Muscle Nerve 29:707–15
    [Google Scholar]
  139. McLoon LK, Wirtschafter J. 2003. Activated satellite cells in extraocular muscles of normal adult monkeys and humans. Investig. Ophthalmol. Vis. Sci. 44:1927–32
    [Google Scholar]
  140. Melendez-Ferro M, Perez-Costas E, Gonzalez MJ, Pombal MA, Anadon R, Rodicio MC. 2000. GABA-immunoreactive internuclear neurons in the ocular motor system of lampreys. Brain Res 855:150–57
    [Google Scholar]
  141. Miles FA 1993. The sensing of rotational and translational optic flow by the primate optokinetic system. Visual Motion and Its Role in the Stabilization of Gaze FA Miles, J Wallman 393–403 Amsterdam: Elsevier
    [Google Scholar]
  142. Miller JM. 2019. EOM pulleys and sequelae: a critical review. Investig. Ophthalmol. Vis. Sci. 60:5052–58
    [Google Scholar]
  143. Moncman CL, Andrade ME, Andrade FH. 2011. Postnatal changes in the developing rat extraocular muscles. Investig. Ophthalmol. Vis. Sci. 52:3962–69
    [Google Scholar]
  144. Morgan DL, Proske U. 1984. Vertebrate slow muscle: its structure, pattern of innervation, and mechanical properties. Physiol. Rev. 64:103–69
    [Google Scholar]
  145. Nguyen LT, Spencer RF. 1999. Abducens internuclear and ascending tract of Deiters inputs to medial rectus motoneurons in the cat oculomotor nucleus: neurotransmitters. J. Comp. Neurol. 411:73–86
    [Google Scholar]
  146. Nieto-Gonzales JL, Carrascal L, Nuñez-Abades P, Torres B. 2007. Phasic and tonic firing properties in rat oculomotor nucleus motoneurons, studied in vitro. Eur. J. Neurosci. 25:2682–96
    [Google Scholar]
  147. Nieto-Gonzalez JL, Carrascal L, Nuñez-Abades P, Torres B. 2009. Muscarinic modulation of recruitment threshold and firing rate in rat oculomotor nucleus motoneurons. J. Neurophysiol. 101:100–11
    [Google Scholar]
  148. Nijssen J, Comley LH, Hedlund E. 2017. Motor neuron vulnerability and resistance in amyotrophic lateral sclerosis. Acta Neuropathol 133:863–85
    [Google Scholar]
  149. Obata K, Highstein SM. 1970. Blocking by picrotoxin of both vestibular inhibition and GABA action on rabbit oculomotor neurons. Brain Res 18:538–41
    [Google Scholar]
  150. O'Brien JA, Berger AJ. 1999. Cotransmission of GABA and glycine to brain stem motoneurons. J. Neurophysiol. 82:1638–41
    [Google Scholar]
  151. Oda K. 1993. Differences in acetylcholine receptor-antibody interactions between extraocular and extremity muscle fibers. Ann. N. Y. Acad. Sci. 681:238–55
    [Google Scholar]
  152. Pastor ÁM, González-Forero D. 2003. Recruitment order of cat abducens motoneurons and internuclear neurons. J. Neurophysiol. 90:2240–52
    [Google Scholar]
  153. Pastor ÁM, Torres B, Delgado-Garcia JM, Baker R. 1991. Discharge characteristics of medial rectus and abducens motoneurons in the goldfish. J. Neurophysiol. 66:2125–40
    [Google Scholar]
  154. Porter JD, Baker RS. 1992. Prenatal morphogenesis of primate extraocular muscle: neuromuscular junction formation and fiber type differentiation. Investig. Ophthalmol. Vis. Sci. 33:657–70
    [Google Scholar]
  155. Porter JD, Baker RS, Ragusa RJ, Brueckner JK. 1995. Extraocular muscles: basic and clinical aspects of structure and function. Surv. Ophthalmol. 39:451–84
    [Google Scholar]
  156. Porter JD, Burns LA, May PJ. 1989. Morphological substrate for eyelid movements: innervation and structure of primate levator palpebrae superioris and orbicularis oculi muscles. J. Comp. Neurol. 287:64–81
    [Google Scholar]
  157. Precht W, Baker R, Okada Y. 1973. Evidence for GABA as the synaptic transmitter of the inhibitory vestibulo-ocular pathway. Exp. Brain Res. 18:415–28
    [Google Scholar]
  158. Priesol AJ, Jones GEG, Tomlinson RD, Broussard D. 2000. Frequency-dependent effects of glutamate antagonists on the vestibulo-ocular reflex of the cat. Brain Res 857:252–64
    [Google Scholar]
  159. Reichenberger I, Straka H, Ottersen OP, Streit P, Gerrits NM, Dieringer N. 1997. Distribution of GABA, glycine and glutamate immunoreactivities in the vestibular nuclear complex of the frog. J. Comp. Neurol. 377:149–64
    [Google Scholar]
  160. Reiner A, Medina L, Figueredocardenas G, Anfinson S. 1995. Brainstem motoneuron pools that are selectively resistant in amyotrophic lateral sclerosis are preferentially enriched in parvalbumin: evidence from monkey brainstem for a calcium-mediated mechanism in sporadic ALS. Exp. Neurol. 131:239–50
    [Google Scholar]
  161. Robinson DA. 1970. Oculomotor unit behavior in the monkey. J. Neurophysiol. 38:393–404
    [Google Scholar]
  162. Roselli F, Caroni P. 2014. Modeling neuronal vulnerability in ALS. Neuron 83:758–60
    [Google Scholar]
  163. Rothstein JD. 2009. Current hypotheses for the underlying biology of amyotrophic lateral sclerosis. Ann. Neurol. 65:Suppl. 1S3–S9
    [Google Scholar]
  164. Rubinstein NA, Hoh JF. 2000. The distribution of myosin heavy chain isoforms among rat extraocular muscle fiber types. Investig. Ophthalmol. Vis. Sci. 41:3391–98
    [Google Scholar]
  165. Rudy B, Maffie J, Amarillo Y, Clark B, Goldberg EM et al. Voltage gated potassium channels: structure and function of Kv1 to Kv9 subfamilies. Encyclopedia of Neuroscience, ed. LR Squire 397–425 New York: Academic
    [Google Scholar]
  166. Rudy B, McBain CJ 2001. Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci 24:517–26
    [Google Scholar]
  167. Ruskell GL. 1999. Extraocular muscle proprioceptors and proprioception. Prog. Retin. Eye Res. 18:269–91
    [Google Scholar]
  168. Ruskell GL, Kjellevold Haugen IB, Bruenech JR, van der Werf F 2005. Double insertions of extraocular rectus muscles in humans and the pulley theory. J. Anat. 206:295–306
    [Google Scholar]
  169. Russier M, Kopysova IL, Ankri N, Ferrand N, Debanne D. 2002. GABA and glycine co-release optimizes functional inhibition in rat brainstem motoneurons in vitro. J. Physiol. 541:123–37
    [Google Scholar]
  170. Russier M, Carlier E, Ankri N, Fronzaroli L, Debanne D. 2003. A-, T-, and H-type currents shape intrinsic firing of developing rat abducens motoneurons. J. Physiol. 549:21–36
    [Google Scholar]
  171. Schiaffino S, Reggiani C. 2011. Fiber types in mammalian skeletal muscles. Physiol. Rev. 91:1447–531
    [Google Scholar]
  172. Schiller PH. 1970. The discharge characteristics of single units in the oculomotor and abducens nuclei of the unanesthetized monkey. Exp. Brain Res. 10:347–62
    [Google Scholar]
  173. Schwaller B. 2014. Calretinin: from a “simple” Ca2+ buffer to a multifunctional protein implicated in many biological processes. Front. Neuroanat. 8:3
    [Google Scholar]
  174. Scott AB, Collins CC. 1973. Division of labor in human extraocular muscle. Arch. Ophthalmol. 90:319–22
    [Google Scholar]
  175. Simpson JI, Leonard CS, Soodak RE. 1988. The accessory optic system: analyzer of self-motion. Ann. N. Y. Acad. Sci. 545:170–79
    [Google Scholar]
  176. Soodak RE, Simpson JI. 1988. The accessory optic system of rabbit. I. Basic visual response properties. J. Neurophysiol. 60:2037–54
    [Google Scholar]
  177. Soupiadou P, Branoner F, Straka H. 2018. Pharmacological profile of vestibular inhibitory inputs to superior oblique motoneurons. J. Neurol. 265:Suppl. 1S18–25
    [Google Scholar]
  178. Spencer RF, Baker R, McCrea RA. 1980. Localization and morphology of cat retractor bulbi motoneurons. J. Neurophysiol. 43:754–70
    [Google Scholar]
  179. Spencer RF, Evinger C, Baker R. 1982. Electron microscopic observations of axon collateral synaptic endings of cat oculomotor motoneurons stained by intracellular injection of horseradish peroxidase. Brain Res 234:423–29
    [Google Scholar]
  180. Spencer RF, Porter JD. 2006. Biological organization of the extraocular muscles. Prog. Brain Res. 151:43–80
    [Google Scholar]
  181. Spencer RF, Wang SF. 1996. Immunohistochemical localization of neurotransmitters utilized by neurons in the rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) that project to the oculomotor and trochlear nuclei in the cat. J. Comp. Neurol. 366:134–48
    [Google Scholar]
  182. Spencer RF, Wenthold RJ, Baker R. 1989. Evidence for glycine as an inhibitory neurotransmitter of vestibular, reticular and prepositus hypoglossi neurons that project to the cat abducens nucleus. J. Neurosci. 9:2718–37
    [Google Scholar]
  183. Stahl JS, Simpson JI. 1995. Dynamics of abducens nucleus neurons in the awake rabbit. J. Neurophysiol. 73:1383–95
    [Google Scholar]
  184. Straka H. 2010. Ontogenetic rules and constraints of vestibulo-ocular reflex development. Curr. Opin. Neurobiol. 20:689–95
    [Google Scholar]
  185. Straka H, Baker R. 2013. Vestibular blueprint in early vertebrates. Front. Neural Circuits 7:182
    [Google Scholar]
  186. Straka H, Dieringer N. 2004. Basic organization principles of the VOR: lessons from frogs. Prog. Neurobiol. 73:259–309
    [Google Scholar]
  187. Straka H, Fritzsch B, Glover JC. 2014. Connecting ears to eye muscles: evolution of a “simple” reflex arc. Brain Behav. Evol. 83:162–75
    [Google Scholar]
  188. Straka H, Gordy C 2020. The vestibular system: the “Leatherman™” among sensory systems. The Senses: A Comprehensive Reference, Vol. 6 B Fritzsch, H Straka 708–20 Amsterdam: Elsevier
    [Google Scholar]
  189. Straka H, Lambert FM, Pfanzelt S, Beraneck M. 2009. Vestibulo-ocular signal transformation in frequency-tuned channels. Ann. N. Y. Acad. Sci. 1164:37–44
    [Google Scholar]
  190. Straka H, Vibert N, Vidal PP, Moore LE, Dutia MB. 2005. Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog. Neurobiol. 76:349–92
    [Google Scholar]
  191. Sturrock RR. 1989. Stability of neuron and glial number in the abducens nerve nucleus of the ageing mouse brain. J. Anat. 166:97–101
    [Google Scholar]
  192. Sugiuchi Y, Takahashi M, Shinoda Y. 2013. Input-output organization of inhibitory neurons in the interstitial nucleus of Cajal projecting to the contralateral trochlear and oculomotor nucleus. J. Neurophysiol. 110:640–57
    [Google Scholar]
  193. Sylvestre PA, Cullen KE. 1999. Quantitative analysis of abducens neuron discharge dynamics during saccadic and slow eye movements. J. Neurophysiol. 82:2612–32
    [Google Scholar]
  194. Tang X, Büttner-Ennever JA, Mustari MJ, Horn AKE. 2015. Internal organization of medial rectus and inferior rectus muscle neurons in the C-group of the oculomotor nucleus in monkey. J. Comp. Neurol. 523:1809–23
    [Google Scholar]
  195. Tjust AE, Danielsson A, Andersen PM, Brännström T, Pedrosa Domellöf F 2017. Impact of amyotrophic lateral sclerosis on slow tonic myofiber composition in human extraocular muscles. Investig. Ophthalmol. Vis. Sci. 58:3708–15
    [Google Scholar]
  196. Tomlinson RD, Robinson DA. 1984. Signals in vestibular nucleus mediating vertical eye movements in the monkey. J. Neurophysiol. 51:1121–36
    [Google Scholar]
  197. Torres-Torrelo J, Rodríguez-Rosell D, Nunez-Abades P, Carrascal L, Torres B. 2012. Glutamate modulates the firing rate in oculomotor nucleus motoneurons as a function of the recruitment threshold current. J. Physiol. 590:3113–27
    [Google Scholar]
  198. Torres-Torrelo J, Torres B, Carrascal L. 2014. Modulation of the input-output function by GABAA receptor-mediated currents in rat oculomotor nucleus motoneurons. J. Physiol. 592:5047–64
    [Google Scholar]
  199. Ugolini G, Klam F, Doldan Dans M, Dubayle D, Brandi AM et al. 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. J. Comp. Neurol. 498:762–85
    [Google Scholar]
  200. Walberg F, Ottersen OP, Rinvik E. 1990. GABA, glycine, aspartate, glutamate and taurine in the vestibular nuclei: an immunocytochemical investigation in the cat. Exp. Brain Res. 79:547–63
    [Google Scholar]
  201. Walls GL. 1962. The evolutionary history of eye movements. Vis. Res. 2:69–80
    [Google Scholar]
  202. Wasicky R, Horn AKE, Büttner-Ennever JA. 2004. Twitch and non-twitch motoneuron subgroups of the medial rectus muscle in the oculomotor nucleus of monkeys receive different afferent projections. J. Comp. Neurol. 479:117–29
    [Google Scholar]
  203. Weiss C, Disterhoft JF. 1985. Connections of the rabbit abducens nucleus. Brain Res 326:172–78
    [Google Scholar]
  204. Wentzel PR, Dezeeuw CI, Holstege JC, Gerrits NM. 1993. Colocalization of GABA and glycine in the rabbit oculomotor nucleus. Neurosci. Lett. 164:25–29
    [Google Scholar]
  205. Zacharias AL, Lewandoski M, Rudnicki MA, Gage PJ. 2011. Pitx2 is an upstream activator of extraocular myogenesis and survival. Dev. Biol. 349:395–405
    [Google Scholar]
  206. Zeeh C, Mayadali ÜS, Horn AKE. 2020. Histochemical characterization of the vestibular Y-group in monkey. Cerebellum https://doi.org/10.1007/s12311-020-01200-z
    [Crossref] [Google Scholar]
  207. Zeeh C, Mustari MJ, Hess BJM, Horn AKE. 2015. Transmitter inputs to different motoneuron subgroups in the oculomotor and trochlear nucleus in monkey. Front. Neuroanat. 9:95
    [Google Scholar]
  208. Zhou Y, Liu D, Kaminski HJ. 2011. Pitx2 regulates myosin heavy chain isoform expression and multi-innervation in extraocular muscle. J. Physiol. 589:4601–14
    [Google Scholar]
  209. Ziermann JM, Diogo R, Noden DM. 2018. Neural crest and the patterning of vertebrate craniofacial muscles. Genesis 56:e23097
    [Google Scholar]
  210. Zimmermann L, Morado-Diaz CJ, Davis-Lopez de Carrizosa MA, de la Cruz RR, May PJ et al. 2013. Axons giving rise to the palisade endings of feline extraocular muscles display motor features. J. Neurosci. 33:2784–93
    [Google Scholar]
/content/journals/10.1146/annurev-vision-100119-125043
Loading
/content/journals/10.1146/annurev-vision-100119-125043
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error