Tectal control of locomotion, steering, and eye movements in lamprey

Journal of Neurophysiology

Volumn 97, Issue 4, 2007, Pages 3093-3108

  Saitoh, Kazuya ^a   Ménard, Ariane ^a   Grillner, Sten ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BEHAVIOR CHANGE; BODY MOVEMENT; BRAIN REGION; CONTROLLED STUDY; ELECTROSTIMULATION; EYE MOVEMENT; LAMPREY; LOCOMOTION; NONHUMAN; OCULOMOTOR SYSTEM; OPTIC TECTUM; PRIORITY JOURNAL; SWIMMING; VESTIBULOOCULAR REFLEX;

ANIMALS; BIOMECHANICS; BRAIN MAPPING; ELECTRIC STIMULATION; EYE MOVEMENTS; LAMPREYS; LOCOMOTION; MODELS, NEUROLOGICAL; MOVEMENT; OCULOMOTOR MUSCLES; ORIENTATION; PSYCHOMOTOR PERFORMANCE; SUPERIOR COLLICULUS; SWIMMING;

EID: 34147170950     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00639.2006     Document Type: Article

References (89)

1. Akert K. Der visuelle Greifreflex. Helv Physiol Acta 7: 112-134, 1949.
2. Al-Akel AS, Guthrie DM, Banks JR. Motor responses to localized electrical stimulation of the tectum in the freshwater perch (Perca fluviatilis). Neuroscience 19: 1381-1391, 1986.
3. Ángeles Luque M, Pilar Pérez-Pérez M, Herrero L, Torres B. Involvement of the optic tectum and mesencephalic reticular formation in the generation of saccadic eye movements in goldfish. Brain Res Brain Res Rev 49: 388-397, 2005.
4. Archambault PS, Deliagina TG, Orlovsky GN. Non-undulatory locomotion in the lamprey. Neuroreport 12: 1803-1807, 2001.
5. Baier H, Klostermann S, Trowe T, Karlstrom RO, Nusslein-Volhard C, Bonhoeffer F. Genetic dissection of the retinotectal projection. Development 123: 415-425, 1996.
6. Beck JC, Gilland E, Tank DW, Baker R. Quantifying the ontogeny of optokinetic and vestibuloocular behaviors in zebrafish, medaka, and goldfish. J Neurophysiol 92: 3546-3561, 2004.
7. Bosch TJ, Paul DH. Differential responses of single reticulospinal cells to spatially localized stimulation of the optic tectum in a teleost fish, Salmo trutta. Eur J Neurosci 5: 742-750, 1993.
8. Budick SA, O'Malley DM. Locomotor repertoire of the larval zebrafish: swimming, turning and prey capture. J Exp Biol 203: 2565-2579, 2000.
9. Carleton SC, Carpenter MB. Afferent and efferent connections of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res 278: 29-51, 1983.
10. Corneil BD, Olivier E, Munoz DP. Neck muscle responses to stimulation of monkey superior colliculus. I. Topography and manipulation of stimulation parameters. J Neurophysiol 88: 1980-1999, 2002.
11. Currie SN, Carlsen RC. Functional significance and neural basis of larval lamprey startle behaviour. J Exp Biol 133: 121-135, 1987.
12. Dean P, Redgrave P, Sahibzada N, Tsuji K. Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19: 367-380, 1986.
13. De Arriba MC, Rodriguez-Alonso M, Pombal MA. Distribution of prosencephalic and mesencephalic afferents in the optic tectum of premetamorphic larvae of petromyzon marinus [Abstract]. FENS Abstr 2: A191.7, 2004.
14. Deliagina TG, Grillner S, Orlovsky GN, Ullén F. Visual input affects the response to roll in reticulospinal neurons of the lamprey. Exp Brain Res 95: 421-428, 1993.
15. Deliagina TG, Ullén F, Gonzalez M-J, Ehrsson H, Orlovsky GN, Grillner S. Initiation of locomotion by lateral line photoreceptors in lamprey: behavioural and neurophysiological studies. J Exp Biol 198: 2581-2591, 1995.
16. Dubuc R, Grillner S. The role of spinal cord inputs in modulating the activity of reticulospinal neurons during fictive locomotion in the lamprey. Brain Res 483: 196-200, 1989.
17. du Lac S, Knudsen EI. Neural maps of head movement vector and speed in the optic tectum of the barn owl. J Neurophysiol 63: 131-146, 1990.
18. Eaton RC, Lee RK, Foreman MB. The Mauthner cell and other identified neurons of the brainstem escape network of fish. Prog Neurobiol 63: 467-485, 2001.
19. El Manira A, Pombal MA, Grillner S. Diencephalic projection to reticulospinal neurons involved in the initiation of locomotion in adult lampreys Lampetra fluviatilis. J Comp Neurol 389: 603-616, 1997.
20. Ewert JP. Neural correlates of key stimulus and releasing mechanism: a case study and two concepts. Trends Neurosci 20: 332-339, 1997.
21. Freedman EG, Stanford TR, Sparks DL. Combined eye-head gaze shifts produced by electrical stimulation of the superior colliculus in rhesus monkeys. J Neurophysiol 76: 927-952, 1996.
22. Fritzsch B, Sonntag R, Dubuc R, Ohta Y, Grillner S. Organization of the six motor nuclei innervating the ocular muscles in lamprey. J Comp Neurol 294: 491-506, 1990.
23. Gahtan E, Tanger P, Baier H. Visual prey capture in larval zebrafish is controlled by identified reticulospinal neurons downstream of the tectum. J Neurosci 25: 9294-9303, 2005.
24. Georgopoulos AP, Grillner S. Visuomotor coordination in reaching and locomotion. Science 245: 1209-1210, 1989.
25. Graham J. An autoradiographic study of the efferent connections of the superior colliculus in the cat. J Comp Neurol 173: 629-654, 1977.
26. Grantyn A, Berthoz A. Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. I. Behavioral properties. Exp Brain Res 66: 339-354, 1987.
27. Grantyn A, Ong-Meang Jacques V, Berthoz A. Reticulo-spinal neurons participating in the control of synergic eye and head movements during orienting in the cat. II. Morphological properties as revealed by intra-axonal injections of horseradish peroxidase. Exp Brain Res 66: 355-377, 1987.
28. Grantyn AA, Dalezios Y, Kitama T, Moschovakis AK. Neuronal mechanisms of two-dimensional orienting movements in the cat. I. A quantitative study of saccades and slow drifts produced in response to the electrical stimulation of the superior colliculus. Brain Res Bull 41: 65-82, 1996.
29. Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4: 573-586, 2003.
30. Grillner S, Hellgren J, Ménard A, Saitoh K, Wikström MA. Mechanisms for selection of basic motor programs - roles for the striatum and pallidum. Trends Neurosci 28: 364-370, 2005.
31. Grillner S, Kashin S. On the generation and performance of swimming in fish. In: Neural Control of Locomotion, edited by Herman RM, Grillner S, Stein P, Stuart DG. New York: Plenum, 1976.
32. Grillner S, Wallén P. How does the lamprey central nervous system make the lamprey swim? J Exp Biol 112: 337-357, 1984.
33. Guimond JC, Auclair F, Lund JP, Dubuc R. Anatomical and physiological study of respiratory motor innervation in lampreys. Neuroscience 122: 259-266, 2003.
34. Guitton D, Crommelinck M, Roucoux A. Stimulation of the superior colliculus in the alert cat. I. Eye movements and neck EMG activity evoked when the head is restrained. Exp Brain Res 39: 63-73, 1980.
35. Herrero L, Rodríguez F, Salas C, Torres B. Tail and eye movements evoked by electrical microstimulation of the optic tectum in goldfish. Exp Brain Res 120: 291-305, 1998.
36. Hikosaka O, Nakamura K, Nakahara H. Basal ganglia orient eyes to reward. J Neurophysiol 95: 567-584, 2006.
37. Hikosaka O, Takikawa Y, Kawagoe R. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80: 953-978, 2000.
38. Ingle DJ. Prey-catching behavior of anurans toward moving and stationary objects. Vision Res Suppl 3: 447-456, 1971.
39. Isa T, Sasaki S. Brainstem control of head movements during orienting; organization of the premotor circuits. Prog Neurobiol 66: 205-241, 2002.
40. Iwahori N, Kawawaki T, Baba J. Neuronal organization of the optic tectum in the river lamprey, Lampetra japonica: a Golgi study. J Hirnforsch 39: 409-424, 1999.
41. Iwahori N, Nakamura K, Tsuda A. Neuronal organization of the optic tectum in the hagfish, Eptatretus burgeri: a Golgi study. Anat Embryol (Berl) 193: 271-279, 1996.
42. 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.
43. Kasicki S, Grillner S. Muller cells and other reticulospinal neurones are phasically active during fictive locomotion in the isolated nervous system of the lamprey. Neurosci Lett 69: 239-243, 1986.
44. Kennedy MC, Rubinson K. Retinal projections in larval, transforming and adult sea lamprey, Petromyzon marinus. J Comp Neurol 171: 465-479, 1977.
45. Kitama T, Ohki Y, Shimazu H, Tanaka M, Yoshida K. Site of interaction between saccade signals and vestibular signals induced by head rotation in the alert cat: functional properties and afferent organization of burster-driving neurons. J Neurophysiol 74: 273-287, 1995.
46. Kostyk SK, Grobstein P. Neuronal organization underlying visually elicited prey orienting in the frog - I. Effects of various unilateral lesions. Neuroscience 21: 41-55, 1987.
47. Kuratani S, Kuraku S, Murakami Y. Lamprey as an evo-devo model: lessons from comparative embryology and molecular phylogenetics. Genesis 34: 175-183, 2002.
48. Lunenburger L, Kleiser R, Stuphorn V, Miller LE, Hoffmann KP. A possible role of the superior colliculus in eye-hand coordination. Prog Brain Res 134: 109-125, 2001.
49. Marin O, Smeets WJ, Gonzalez A. Evolution of the basal ganglia in tetrapods: a new perspective based on recent studies in amphibians. Trends Neurosci 21: 487-494, 1998.
50. McClellan AD, Grillner S. Initiation and sensory gating of "fictive" swimming and withdrawal responses in an in vitro preparation of the lamprey spinal cord. Brain Res 269: 237-250, 1983.
51. McIlwain JT. Effects of eye position on saccades evoked electrically from superior colliculus of alert cats. J Neurophysiol 55: 97-112, 1986.
52. Meek J. Functional anatomy of the tectum mesencephali of the goldfish. An explorative analysis of the functional implications of the laminar structural organization of the tectum. Brain Res 287: 247-297, 1983.
53. Ménard A, Auclair F, Bourcier C, Grillner S, Dubuc R. Descending GABA inputs to the mesencephalic locomotor region of the lamprey [Abstract]. FENS Abstr 4: A182.4, 2006.
54. Meyer RL. Mapping the normal and regenerating retinotectal projection of goldfish with autoradiographic methods. J Comp Neurol 189: 273-289, 1980.
55. Moschovakis AK, Scudder CA, Highstein SM. The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol 50: 133-254, 1996.
56. Munoz DP, Guitton D, Pelisson D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J Neurophysiol 66: 1642-1666, 1991.
57. Muto N, Kakei S, Shinoda Y. Morphology of single axons of tectospinal neurons in the upper cervical spinal cord. J Comp Neurol 372: 9-26, 1996.
58. New JG, Alborg Fewkes L, Khan AN. Strike feeding behavior in the muskellunge, Esox masquinongy: contributions of the lateral line and visual sensory systems. J Exp Biol 204: 1207-1221, 2001.
59. Nieuwenhuys R, Nicholson C. Lampreys, Petromyzontoidea. In: The Central Nervous System of Vertebrates, edited by Nicholson C. Berlin: Springer-Verlag, 1998.
60. Olivier E, Grantyn A, Chat M, Berthoz A. The control of slow orienting eye movements by tectoreticulospinal neurons in the cat: behavior, discharge patterns and underlying connections. Exp Brain Res 93: 435-449, 1993.
61. Peterson BW. Current approaches and future directions to understanding control of head movement. Prog Brain Res 143: 369-381, 2004.
62. Pettigrew JD, Collin SP, Fritsches K. Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei). J Comp Physiol A Sens Neural Behav Physiol 186: 247-260, 2000.
63. Redgrave P, Mitchell IJ, Dean P. Descending projections from the superior colliculus in rat: a study using orthograde transport of wheatgerm-agglutinin conjugated horseradish peroxidase. Exp Brain Res 68: 147-167, 1987.
64. Rice AN, Westneat MW. Coordination of feeding, locomotor and visual systems in parrotfishes (Teleostei: Labridae). J Exp Biol 208: 3503-3518, 2005.
65. Rio JP, Vesselkin NP, Reperant J, Kenigfest NB, Miceli D, Adanina V. Retinal and non-retinal inputs upon retinopetal RMA neurons in the lamprey: a light and electron microscopic study combining HRP axonal tracing and GABA immunocytochemistry. J Chem Neuroanat 12: 51-70, 1996.
66. Robertson B, Saitoh K, Ménard A, Grillner S. Afferents of the lamprey optic tectum with special reference to the GABAergic input: a combined tracing and immunohistochemical study. J Comp Neurol 499: 106-119, 2006.
67. Robinson DA. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res 12: 1795-1808, 1972.
68. Roeser T, Baier H. Visuomotor behaviors in larval zebrafish after GFP-guided laser ablation of the optic tectum. J Neurosci 23: 3726-3734, 2003.
69. Roucoux A, Guitton D, Crommelinck M. Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Exp Brain Res 39: 75-85, 1980.
70. Rovainen CM. Neurobiology of lampreys. Physiol Rev 59: 1007-1077, 1979.
71. Sahibzada N, Dean P, Redgrave P. Movements resembling orientation or avoidance elicited by electrical stimulation of the superior colliculus in rats. J Neurosci 6: 723-733, 1986.
72. Saitoh K, Ménard A, Grillner S. Coordination of eye and locomotor movement elicited from the lamprey tectum. Soc Neurosci Abstr 882.6, 2004.
73. Sajovic P, Levinthal C. Visual cells of zebrafish optic tectum: mapping with small spots. Neuroscience 7: 2407-2426, 1982.
74. Salas C, Herrero L, Rodríguez F, Torres B. Tectal codification of eye movements in goldfish studied by electrical microstimulation. Neuroscience 78: 271-288, 1997.
75. Sasaki S, Yoshimura K, Naito K. The neural control of orienting: role of multiple-branching reticulospinal neurons. Prog Brain Res 143: 383-389, 2004.
76. Schiller PH, Stryker M. Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J Neurophysiol 35: 915-924, 1972.
77. Schwassman HO, Kruger L. Organization of the visual projection upon the optic tectum of some freshwater fish. J Comp Neurol 124: 113-126, 1965.
78. Sparks DL. The brainstem control of saccadic eye movements. Nat Rev Neurosci 3: 952-964, 2002.
79. Stanford TR, Freedman EG, Sparks DL. Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J Neurophysiol 76: 3360-3381, 1996.
80. Stein BE, Goldberg SJ, Clamann HP. The control of eye movements by the superior colliculus in the alert cat. Brain Res 118: 469-474, 1976.
81. Stryker MP, Schiller PH. Eye and head movements evoked by electrical stimulation of monkey superior colliculus. Exp Brain Res 23: 103-112, 1975.
82. Stuermer CA. Retinotopic organization of the developing retinotectal projection in the zebrafish embryo. J Neurosci 8: 4513-4530, 1988.
83. Stuermer CA, Raymond PA. Developing retinotectal projection in larval goldfish. J Comp Neurol 281: 630-640, 1989.
84. Tabak S, Smeets JB, Collewijn H. Modulation of the human vestibuloocular reflex during saccades: probing by high-frequency oscillation and torque pulses of the head. J Neurophysiol 76: 3249-3263, 1996.
85. Ullén F, Deliagina TG, Orlovsky GN, Grillner S. Spatial orientation in the lamprey. J Exp Biol 198: 675-681, 1995.
86. Vinay L, Grillner S. The spino-reticulo-spinal loop can slow down the NMDA-activated spinal locomotor network in lamprey. Neuroreport 4: 609-612, 1993.
87. Warton SS, Jones DG. Postnatal development of the superficial layers in the rat superior colliculus: a study with Golgi-Cox and Kluver-Barrera techniques. Exp Brain Res 58: 490-502, 1985.
88. Zompa IC, Dubuc R. A mesencephalic relay for visual inputs to reticulospinal neurones in lampreys. Brain Res 718: 221-227, 1996.
89. Zompa IC, Dubuc R. Electrophysiological and neuropharmacological study of tectoreticular pathways in lampreys. Brain Res 804: 238-252, 1998.