Input-output organization of inhibitory neurons in the interstitial nucleus of Cajal projecting to the contralateral trochlear and oculomotor nucleus

Journal of Neurophysiology

Volumn 110, Issue 3, 2013, Pages 640-657

  Sugiuchi, Y ^a   Takahashi, M ^a   Shinoda, Y ^a  

^a TOKYO MEDICAL AND DENTAL UNIVERSITY   (Japan)

Author keywords

Inhibitory burst neuron; Interstitial nucleus of Cajal; Saccade; Superior colliculus; Vertical

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CAT; CONTROLLED STUDY; EYE MOVEMENT; HEAD MOVEMENT; INFERIOR RECTUS MOTONEURON; INTERSTITIAL CELL OF CAJAL; INTRACELLULAR RECORDING; MONOSYNAPTIC POTENTIAL; MOTONEURON; NERVE CELL; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NERVE PROJECTION; NONHUMAN; OCULOMOTOR NUCLEUS; PRIORITY JOURNAL; SOMATOSENSORY SYSTEM; SUPERIOR COLLICULUS; SYNAPTIC INHIBITION; TROCHLEAR NUCLEUS;

EID: 84880977839     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01045.2012     Document Type: Article

References (98)

1. Akagi Y. The location of the motor neurons innervating the extraocular muscles in the oculomotor nuclei of the cat and rabbit, using horseradish peroxidase. J Comp Neurol 181: 745-762, 1978.
2. Altman J, Carpenter MB. Fiber projections of the superior colliculus in the cat. J Comp Neurol 116: 157-177, 1961.
3. Benevento L, Rezak M, Santos-Anderson R. An autoradiographic study of the projections of the pretectum in the rhesus monkey (Macaca mulatta): evidence for sensorimotor links to the thalamus and oculomotor nuclei. Brain Res 127: 197-218, 1977.
4. Berman N. Connections of the pretectum in the cat. J Comp Neurol 174: 227-254, 1977.
5. Büttner U, Büttner-Ennever JA, Henn V. Vertical eye movement related unit activity in the rostral mesencephalic reticular formation of the alert monkey. Brain Res 130: 239-252, 1977.
6. Büttner-Ennever JA, Büttner U. A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Res 151: 31-47, 1978.
7. Büttner-Ennever JA, Büttner U. The reticular formation. In: Reviews of Oculomotor Research, Neuroanatomy of the Oculomotor System, edited by Büttner-Ennever JA. Amsterdam: Elsevier, 1988, p. 119-176.
8. Büttner-Ennever JA, Büttner U, Cohen B, Baumgartner G. Vertical gaze paralysis and the rostral interstitial nucleus of the medial longitudinal fasciculus. Brain 105: 125-149, 1982.
9. 125I]B-IIb tetanus toxin fragment. Ann N Y Acad Sci 374: 157-170, 1981.
10. Carpenter MB, Harbison JW, Peter P. Accessory oculomotor nuclei in the monkey: projections and effects of discrete lesions. J Comp Neurol 140: 131-154, 1970.
11. Chen B, May PJ. Premotor circuits controlling eyelid movements in conjunction with vertical saccades in the cat. II. Interstitial nucleus of Cajal. J Comp Neurol 500: 676-692, 2007.
12. Chimoto S, Iwamoto Y, Yoshida K. Projections of vertical eye movement-related neurons in the interstitial nucleus of Cajal to the vestibular nucleus in the cat. Neurosci Res 15: 293-298, 1992.
13. Chimoto S, Iwamoto Y, Yoshida K. Projections and firing properties of down eye-movement neurons in the interstitial nucleus of Cajal in the cat. J Neurophysiol 81: 1199-1211, 1999.
14. Cohen B, Henn V. Unit activity in the pontine reticular formation associated with eye movements. Brain Res 46: 403-410, 1972.
15. Crawford JD, Vilis T. Modularity and parallel processing in the oculomotor integrator. Exp Brain Res 96: 443-456, 1993.
16. Eccles JC. The Physiology of Synapses. Berlin: Springer-Verlag, 1964.
17. Edwards SB. The commissural projection of the superior colliculus in the cat. J Comp Neurol 173: 23-40, 1977.
18. Edwards SB, Henkel CK. Superior colliculus connections with the extraoc-ular motor nuclei in the cat. J Comp Neurol 179: 451-467, 1978.
19. Evinger C. Extraocular motor nuclei: location, morphology, and afferents. In: Neuroanatomy of the Oculomotor System, edited by Büttner-Ennever JA. Amsterdam: Elsevier, 1988, p. 81-117.
20. Fukushima K. The interstitial nucleus of Cajal and its role in the control of movements of head and eyes. Prog Neurobiol 29: 107-192, 1987.
21. Fukushima K. The interstitial nucleus of Cajal in the midbrain reticular formation and vertical eye movement. Neurosci Res Suppl 10: 159-187, 1991.
22. Fukushima K, Kaneko CR. Vestibular integrators in the oculomotor system. Neurosci Res 22: 249-258, 1995.
23. Fukushima K, Harada C, Fukushima J, Suzuki Y. Spatial properties of vertical eye movement-related neurons in the region of the interstitial nucleus of Cajal in awake cats. Exp Brain Res 79: 25-42, 1990a.
24. Fukushima K, Fukushima J, Harada C, Ohashi T, Kase M. Neuronal activity related to vertical eye movement in the region of the interstitial nucleus of Cajal in alert cats. Exp Brain Res 79: 43-64, 1990b.
25. Fukushima K, Fukushima J, Ohashi T, Kase M. Possible downward burster-driving neurons related to the anterior semicircular canal in the region of the interstitial nucleus of Cajal in alert cats. Neurosci Res Suppl 12: 536-544, 1991.
26. Fukushima K, Kaneko CR, Fuchs AF. The neuronal substrate of integration in the oculomotor system. Prog Neurobiol 39: 609-639, 1992.
27. Fukushima K, Ohashi T, Fukushima J, Kaneko CR. Discharge characteristics of vestibular and saccade neurons in the rostral midbrain of alert cats. J Neurophysiol 73: 2129-2143, 1995.
28. Graf W, McCrea RA, Baker R. Morphology of posterior canal related secondary vestibular neurons in rabbit and cat. Exp Brain Res 52: 125-138, 1983.
29. Graham J. An autoradiographic study of the efferent connections of the superior colliculus in the cat. J Comp Neurol 173: 629-654, 1977.
30. Grantyn A, Grantyn R. Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tecto-bulbo-spinal tract. Exp Brain Res 46: 243-256, 1982.
31. Grantyn AA, Moschovakis AK. Structure-function relationships in the superior colliculus of higher mammals. In: The Superior Colliculus: New Approaches for Studying Sensorimotor Integration, edited by Hall WC, Moschovakis A. Boca Raton, Florida: CRC Press, 2004, p. 107-145.
32. Graybiel AM, Hartwieg EA. Some afferent connections of the oculomotor complex in the cat: an experimental study with tracer techniques. Brain Res 81: 543-551, 1974.
33. Harting JK, Huerta MF, Frankfurter AJ, Strominger NL, Royce GJ. Ascending pathways from the monkey superior colliculus: an autoradio-graphic analysis. J Comp Neurol 192: 853-882, 1980.
34. Hassler R. Supranuclear structures regulating binocular eye and head movements. In: Cerebral Control of Eye Movements and Motion Perception. Bibiotheca Ophthalmol No. 82. Basel: Kager, 1972, p. 207-220.
35. Helmchen C, Rambold H, Büttner U. Saccade-related burst neurons with torsional and vertical on-directions in the interstitial nucleus of Cajal of the alert monkey. Exp Brain Res 112: 63-78, 1996.
36. Helmchen C, Rambold H, Fuhry L, Büttner U. 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: 436-452, 1998.
37. Henn V. Pathophysiology of rapid eye movements in the horizontal, vertical and torsional directions. Baillieres Clin Neurol 1: 373-391, 1992.
38. Hepp K, Vilis T, Henn V. On the generation of rapid eye movements in three dimensions. Ann N Y Acad Sci 545: 140-153, 1988.
39. Hepp K, Henn V, Vilis T, Cohen B. Brainstem regions related to saccade generation. In: The Neurobiology of Saccadic Eye Movements. Reviews of Oculomotor Research, edited by Wurtz RH, Goldberg ME. Amsterdam: Elsevier, 1989, p. 105-212.
40. Hess WR. Das Zwischenhirn: Syndrome, Localizationen Funktionen. Basel: Schwabe, 1954.
41. Hikosaka O, Kawakami T. Inhibitory reticular neurons related to the quick phase of vestibular nystagmus. Their location and projection. Exp Brain Res 27: 377-396, 1977.
42. Hoffmann KP, Straschill M. Influence of cortico-tectal and intertectal connections on visual responses in the cat's superior colliculus. Exp Eye Res 12: 120-131, 1971.
43. Horn AK, Büttner-Ennever JA. Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification by parvalbumin immunostaining. J Comp Neurol 392: 413-427, 1998.
44. Infante C, Leiva J. Simultaneous unitary activity in both superior colliculi and its relation to eye movements in the cat. Brain Res 381: 390-392, 1986.
45. Isa T, Hall WC. Exploring the superior colliculus in vitro. J Neurophysiol 102: 2581-2593, 2009.
46. Itoh K. Efferent projection of the pretectum of cat. Exp Brain Res 30: 89-105, 1977.
47. Iwamoto Y, Kitama T, Yoshida K. Vertical eye movement-related secondary vestibular neurons ascending in medial longitudinal fasciculus in cat. II. Direct connections with extraocular motoneurons. J Neurophysiol 63: 918-935, 1990.
48. Izawa Y, Sugiuchi Y, Shinoda Y. Neural organization from the superior colliculus to motoneurons in the horizontal oculomotor system of the cat. J Neurophysiol 81: 2597-2611, 1999.
49. Izawa Y, Sugiuchi Y, Shinoda Y. Neural organization of the pathways from the superior colliculus to trochlear motoneurons. J Neurophysiol 97: 3696-3712. 2007.
50. Kaneko CR, Fukushima K. Discharge characteristics of vestibular saccade neurons in alert monkeys. J Neurophysiol 79: 835-847, 1998.
51. Kawamura K, Hashikawa T. Cell bodies of origin of reticular projections from the superior colliculus in the cat: an experimental study with the use of horseradish peroxidase as a tracer. J Comp Neurol 182: 1-16, 1978.
52. Keller EL. Participation of medial pontine reticular formation in eye movement generation in monkey. J Neurophysiol 37: 316-332, 1974.
53. King WM, Fuchs AF. Neuronal activity in the mesencephalon related to vertical eye movements. In: Control of Gaze by Brainstem Neurons, Developments in Neuroscience, edited by Baker R, Berthoz A. Amsterdam: Elsevier, 1977, p. 319-326.
54. King WM, Fuchs AF. Reticular control of vertical saccadic eye movements by mesencephalic burst neurons. J Neurophysiol 42: 861-876, 1979.
55. King WM, Fuchs AF, Magnin M. Vertical eye movement-related responses of neurons in midbrain near interstitial nucleus of Cajal. J Neurophysiol 46: 549-562, 1981.
56. King WM, Precht W, Dieringer N. Synaptic organization of frontal eye field and vestibular afferents to interstitial nucleus of Cajal in the cat. J Neuro-physiol 43: 912-928, 1980.
57. Kokkoroyannis T, Scudder CA, Balaban CD, Highstein SM, Moschovakis AK. Anatomy and physiology of the primate interstitial nucleus of Cajal. I. Efferent projections. J Neurophysiol 75: 725-739, 1996.
58. Luschei E, Fuchs AF. Activity of brainstem neurons during eye movements of alert monkeys. J Neurophysiol 35: 445-461, 1972.
59. Maeda M, Shibazaki T, Yoshida K. Monosynaptic inhibition evoked in superior colliculus neurons following contralateral collicular stimulation. In: Integrative Control Functions of the Brain, edited by Ito M. Amsterdam: Elsevier, North-Holland Biomedical, 1979, p. 68-71.
60. Mabuchi M, Kusama T. Mesodiencephalic projections to the inferior olive and the vestibular and perihypoglossal nuclei. Brain Res 1970: 133-136, 1970.
61. Markham CH, Precht W, Shimazu H. Effect of stimulation of interstitial nucleus of Cajal on vestibular unit activity in the cat. J Neurophysiol 29: 493-507, 1966.
62. May PJ. The mammalian superior colliculus: laminar structure and connections. Prog Brain Res 151: 321-378, 2006.
63. McIlwain JT. Effects of eye position on saccades evoked electrically from superior colliculus of alert cats. J Neurophysiol 55: 97-112, 1986.
64. Mesulam MM. Tetramethyl benzidine horseradish peroxidase neurohisto-chemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents. J Hirnforsch 26: 106-117, 1978.
65. Moschovakis AK, Karabelas AB. Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. J Comp Neurol 239: 276-308, 1985.
66. Moschovakis AK, Scudder CA, Highstein SM. Structure of the primate oculomotor burst generator. I. Medium-lead burst neurons with upward on-direction. J Neurophysiol 65: 203-217, 1991a.
67. Moschovakis AK, Scudder CA, Highstein SM, Warren JD. Structure of the primate oculomotor burst generator. II. Medium-lead burst neurons with downward on-direction. J Neurophysiol 65: 218-229, 1991b.
68. Nakamagoe K, Iwamoto Y, Yoshida K. Evidence for brainstem structures participating in oculomotor integration. Science 288: 857-859, 2000.
69. Nakao S, Shiraishi Y. Excitatory and inhibitory synaptic inputs from the medial mesodiencephalic junction to vertical eye movement-related mo-toneurons in the cat oculomotor nucleus. Neurosci Lett 42: 125-130, 1983.
70. Nakao S, Shiraishi Y. Direct excitatory and inhibitory synaptic inputs from the medial mesodiencephalic junction to motoneurons innervating extraoc-ular oblique muscles in the cat. Exp Brain Res 61: 62-72, 1985.
71. Ohki Y, Shimazu H, Suzuki I. Excitatory input to burst neurons from the labyrinth and its mediating pathway in the cat: location and functional characteristics of burster-driving neurons. Exp Brain Res 72: 457-472, 1988.
72. Onodera S. Olivary projections from the mesodiencephlic structures in the cat studied by means of axonal transport of horseradish peroxidase and tritiated amino acids. J Comp Neurol 227: 37-49, 1984.
73. Panneton WM, Martin GF. Midbrain projections to the trigeminal, facial and hypoglossal nuclei in the opossum. A study using axonal transport techniques. Brain Res 168: 493-511, 1979.
74. Pompeiano O, Walberg F. Descending connections to the vestibular nuclei. An experimental study in the cat. J Comp Neurol 108: 465-503, 1957.
75. Precht W, Schwindt PC, Magherini PC. Tectal influences on cat ocular motoneurons. Brain Res 82: 27-40, 1974.
76. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98: 417-440, 1975.
77. Roucoux A, Crommelinck M. Eye movements evoked by superior colliculus stimulation in the alert cat. Exp Brain Res 106: 349-363, 1976.
78. Sasaki K, Kawaguchi S, Matsuda Y, Mizuno N. Electrophysiological studies on cerebello-cerebral projections in the cat. Exp Brain Res 16: 75-88, 1972.
79. Sasaki K, Staunton HP, Dieckmann G. Characteristic features of augmenting and recruiting responses in the cerebral cortex. Exp Neurol 26: 369-392, 1970.
80. Schiller PH, Körner F. Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. J Neurophysiol 34: 920-936, 1971.
81. Schwindt PC, Precht W, Richter A. Monosynaptic excitatory and inhibitory pathways from medial midbrain nuclei to trochlear motoneurons. Exp Brain Res 20: 223-228, 1974.
82. Scudder CA, Kaneko CR, Fuchs AF. The brainstem burst generator for saccadic eye movements. A modern synthesis. Exp Brain Res 142: 439-462, 2002.
83. Shinoda Y, Ghez C, Arnold A. Spinal branching of rubrospinal axons in the cat. Exp Brain Res 30: 203-218, 1977.
84. Shiraishi Y, Nakao S. Differential locations in the midbrain of distinct groups of vertical eye movement-related neurones in cat: their projections and direct connections with oculomotor neurones. Acta Physiol Scand 154: 151-163, 1995. [Erratum. Acta Physiol Scand 155 (Sept): 111, 1995.]
85. Sparks DL. Conceptual issues related to the role of the superior colliculus in the control of gaze. Curr Opin Neurobiol 9: 698-707, 1999.
86. Steiger HJ, Büttner-Ennever JA. Oculomotor nucleus afferents in the monkey demonstrated with horseradish peroxidase. Brain Res 160: 1-15, 1979.
87. Sugiuchi Y, Izawa Y, Takahashi M, Na J, Shinoda Y. Physiological characterization of synaptic inputs to inhibitory burst neurons from the rostral and caudal superior colliculus. J Neurophysiol 93: 697-712, 2005.
88. Sugiuchi Y, Takahashi M, Izawa Y, Shinoda Y. Input-output organization of inhibitory burst neurons in the interstitial nucleus of Cajal. Ann N Y Acad Sci 1233, Suppl: 133-151, 2011.
89. Szentágothai J. Die zentrale innervations der Augenbewegungen. Arch Psy-chiatr Nervenkr 116: 1943.
90. Takahashi M, Sugiuchi Y, Izawa Y, Shinoda Y. Commissural excitation and inhibition of the superior colliculus on tectoreticular neurons projecting to omnipause neuron and inhibitory burst neuron regions. J Neurophysiol 94: 1707-1726, 2005.
91. Takahashi M, Sugiuchi Y, Shinoda Y. Commissural mirror-symmetric excitation and reciprocal inhibition between the two superior colliculi and their roles in vertical and horizontal eye movements. J Neurophysiol 98: 2664-2682, 2007.
92. Takahashi M, Sugiuchi Y, Shinoda Y. Topographic organization of excitatory and inhibitory commissural connections in the superior colliculi and their functional roles in saccade generation. J Neurophysiol 104: 3146-3167, 2010.
93. Takahashi M, Sugiuchi Y, Shinoda Y. Commissural inhibition between bilateral superior colliculi for saccades and bilateral vestibular nuclei for vestibulo-ocular reflex (VOR). Ann N Y Acad Sci 1233, Suppl: 152-174, 2011.
94. Wang SH, Spencer RF. Spatial organization of premotor neurons related to vertical upward and downward saccadic eye movements in the rostral interstitial nucleus of the medial longitudinal fasciculus (ri MLF) in the cat. J Comp Neurol 366: 163-180, 1996.
95. Weber JT, Harting JK. The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis. Brain Res 194: 1-28, 1980.
96. Wurtz RH, Goldberg ME. Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. J Neurophysiol 35: 575-586, 1972.
97. Yoshida K, McCrea R, Berthoz A, Vidal PP. Morphological and physiological characteristics of inhibitory burst neurons controlling horizontal rapid eye movements in the alert cat. J Neurophysiol 48: 761-784, 1982.
98. Zuk A, Gwyn DG, Rutherford JG. Cytoarchitecture, neuronal morphology, and some efferent connections of the interstitial nucleus of Cajal (INC) in the cat. J Comp Neurol 212: 278-292, 1982.