Inhibition of superior colliculus neurons by a GABAergic input from the pretectal nuclear complex in the rat

European Journal of Neuroscience

Volumn 20, Issue 12, 2004, Pages 3404-3412

  Born, Gesche ^a   Schmidt, Matthias ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

GABA; GABA receptors; Inhibition; Pretectum; Saccades

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID;

ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELL STRUCTURE; CONTROLLED STUDY; DENDRITIC CELL; ELECTROPHYSIOLOGY; GABAERGIC TRANSMISSION; IN VITRO STUDY; INFORMATION PROCESSING; NERVE PROJECTION; NONHUMAN; PATCH CLAMP; POSTSYNAPTIC MEMBRANE; PRETECTAL NUCLEAR COMPLEX; PRETECTUM; PRIORITY JOURNAL; RAT; SUPERIOR COLLICULUS; VISION; VISUAL CORTEX; VISUOMOTOR COORDINATION;

ANIMALS; BICUCULLINE; FEMALE; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MALE; NEURAL INHIBITION; NEURONS; RATS; RATS, LONG-EVANS; SUPERIOR COLLICULUS; SYNAPTIC TRANSMISSION;

EID: 10944233650     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03820.x     Document Type: Article

References (59)

1. Albano, J.E., Norton, T.T. & Hall, W.C. (1979) Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis. Brain Res., 173, 1-11.
2. Appell, P.P. & Behan, M. (1990) Sources of subcortical GABAergic projections to the superior colliculus in the cat. J. Comp. Neurol., 302, 143-158.
3. Araki, M., McGeer, P. & McGeer, E. (1984) Presumptive gamma-aminobutyric acid pathways from the midbrain to the superior colliculus studied by a combined horseradish peroxidase gamma-aminobutyric acid transaminase pharmacohistochemical method. Neuroscience, 13, 433-439.
4. Baldauf, Z.B., Wang, X.P., Wang, S. & Bickford, M.E. (2003) Pretectotectal pathway: an ultrastructural quantitative analysis in cats. J. Comp. Neurol., 464, 141-158.
5. Ballas, I. & Hoffmann, K.P. (1985) A correlation between receptive field properties and morphological structures in the pretecrum of the cat. J. Comp. Neurol., 238, 417-428.
6. Büttner-Ennever, J.A., Cohen, B., Horn, A.K.E. & Reisine, H. (1996) Efferent pathways of the nucleus of the optic tract in monkey and their role in eye movements. J. Comp. Neurol., 373, 90-107.
7. Cadusseau, J. & Roger, M. (1985) Afferent projections to the superior colliculus in the rat, with special attention to the deep layers. J. Hirnforsch., 26, 667-681.
8. Caldwell, R.B. & Mize, R.R. (1980) Superior colliculus neurons which project to the cat lateral posterior nucleus have varying morphologies. J. Comp. Neurol., 203, 53-66.
9. Cazin, L., Precht, W. & Lannou, J. (1980) Firing characteristics of neurons mediating optokinetic responses to rat's vestibular neurons. Pflügers Arch., 383, 221-230.
10. Clarke, R.J., Zhang, H. & Gamlin, P.D. (2003) Primate pupillary light reflex: receptive field characteristics of pretectal luminance neurons. J. Neurophysiol., 89, 3168-3178.
11. Cohen, B., Reisine, H., Yokota, J.I. & Raphan, T. (1992) The nucleus of the optic tract. Its function in gaze stabilization and control of visual-vestibular interaction. Ann. NY Acad. Sci., 656, 277-296.
12. Collewijn, H. (1975) Direction-selective units in the rabbit's nucleus of the optic tract. Brain Res., 100, 489-508.
13. Cucchiaro, J.B., Bickford, M.E. & Sherman, S.M. (1991) A GABAergic projection from the pretectum to the dorsal lateral geniculate nucleus in the cat. Neuroscience, 41, 213-226.
14. Cucchiaro, J.B., Uhlrich, D.J. & Sherman, S.M. (1993) Ultrastructure of synapses from the pretectum in the A-laminae of the cat's lateral geniculate nucleus. J. Comp. Neurol., 334, 618-630.
15. Distler, C. & Hoffmann, K.P. (1989a) The pupillary light reflex in normal and innate microstrabismic cats, I: Behavior and receptive-field analysis in the nucleus praetectalis olivaris. Vis. Neurosci., 3, 127-138.
16. Distler, C. & Hoffmann, K.P. (1989b) The pupillary light reflex in normal and innate microstrabismic cats, II: Retinal and cortical input to the nucleus praetectalis olivaris. Vis. Neurosci., 3, 139-153.
17. Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stein, B.E. (1979) Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol., 184, 309-329.
18. Ficalora, A. & Mize, R.R. (1989) The neurons of the substantia nigra and zona incerta which project to the cat superior colliculus are GABA immunoreactive - a double-label study using GABA immunocytochemistry and lectin retrograde transport. Neuroscience, 29, 567-581.
19. Fischer, W.H., Schmidt, M. & Hoffmann, K.P. (1998) Saccade-induced activity of dorsal lateral geniculate nucleus X- and Y-cells during pharmacological inactivation of the cat pretectum. Vis. Neurosci., 15, 197-210.
20. Fuchs, A.F., Mustari, M.J., Robinson, F.R. & Kaneko, C.R. (1992) Visual signals in the nucleus of the optic tract and their brain stem destinations. Ann. N Y Acad. Sci., 76, 266-276.
21. Gamlin, P.D., Zhang, H. & Clarke, R.J. (1995) Luminance neurons in the pretectal olivary nucleus mediate the pupillary light reflex in the rhesus monkey. Exp. Brain Res., 106, 169-176.
22. Graham, J. (1977) An autoradiographic study of the of the efferent connections of the superior colliculus in the cat. J. Comp. Neurol., 173, 629-654.
23. Graham, J. & Casagrande, V.A. (1980) A light microscope and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). J. Comp. Neurol., 191, 133-151.
24. Harrell, J.V., Caldwell, R.B. & Mize, R.R. (1982) The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat. Exp. Brain Res., 46, 234-242.
25. Hoffmann, K.P., Behrend, K. & Schoppmann, A. (1976) A direct afferent visual pathway from the nucleus of the optic tract to the inferior olive in the cat. Brain Res., 115, 150-153.
26. Hoffmann, K.P. & Distler, C. (1989) Quantitative analysis of visual receptive fields of neurons in nucleus of the optic tract and dorsal terminal nucleus of the accessory optic tract in macaque monkey. J. Neurophysiol., 62, 416-428.
27. Hoffmann, K.P. & Schoppmann, A. (1981) A quantitative analysis of the direction-specific response of neurons in the cat's nucleus of the optic tract. Exp. Brain Res., 42, 146-157.
28. Holstege, G. & Collewijn, H. (1982) The efferent connections of the nucleus of the optic tract and the superior colliculus in the rabbit. J. Comp. Neurol., 209, 139-175.
29. Kato, I., Harada, K., Hasegawa, T., Igarashi, T., Koike, Y. & Kawasaki, T. (1986) Role of the nucleus of the optic tract in monkeys in relation to optokinetic nystagmus. Brain Res., 364, 12-22.
30. Kato, I., Watanabe, S., Sato, S. & Norita, M. (1995) Pretectofugal fibers from the nucleus of the optic tract in monkeys. Brain Res., 705, 109-117.
31. Klooster, J., Vrensen, G.F., Muller, L.J. & Van der Want, J.J. (1995) Efferent projections of the olivary pretectal nucleus in the albino rat subserving the pupillary light reflex and related reflexes. A light microscopic tracing study. Brain Res., 688, 34-46.
32. Kourouyan, H.D. & Horton, J.C. (1997) Transneuronal retinal input to the primate Edinger-Westphal nucleus. J. Comp. Neurol., 381, 68-80.
33. Kubota, T., Morimoto, M., Kanaseki, T. & Inomato, H. (1989) Projection from the superficial layers of the tectum to the pretectal complex in the cat. Brain Res. Bull., 22, 373-378.
34. Langer, T.P. & Lund, R.D. (1974) The upper layers of the superior colliculus of the rat: a Golgi study. J. Comp. Neurol., 158, 418-435.
35. Lee, C., Rohrer, W.H. & Sparks, D.L. (1988) Population coding of saccadic eye movements by neurons in the superior colliculus. Nature, 332, 357-360.
36. Lugo-Garcia, N. & Kicliter, E. (1987) Superior colliculus efferents to five subcortical visual system structures in the ground squirrel. Brain Res., 426, 131-141.
37. Missal, M., Coimbra, A., Lefevre, P. & Olivier, E. (2002) A quantitative analysis of the correlations between eye movements and neural activity in the pretectum. Exp. Brain Res., 143, 373-382.
38. Mize, R.R. (1988) Immunocytochemical localization of γ-aminobutyric acid (GABA) in the superior colliculus. J. Comp. Neurol., 276, 169-187.
39. Mize, R.R. (1992) The organization of GABAergic neurons in the mammalian superior colliculus. Prog. Brain Res., 90, 219-248.
40. Mize, R.R., Spencer, R.F. & Sterling, P. (1982) Two types of GABA-accumulating neurons in the superficial gray layer of the cat superior colliculus. J. Comp. Neurol., 206, 180-192.
41. Morin, L.P. & Blanchard, J.H. (1998) Interconnections among nuclei of the subcortical visual shell: the intergeniculate leaflet is a major constituent of the hamster subcortical visual system. J. Comp. Neurol., 396, 288-309.
42. Munoz, D.P. & Wurtz, R.H. (1995a) Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol., 73, 2313-2333.
43. Munoz, D.P. & Wurtz, R.H. (1995b) Saccade-related activity in monkey superior colliculus. II. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol., 73, 2334-2348.
44. Nunes Cardozo, B., Mize, R.R. & Van der Want, J.J. (1994) GABAergic and non-GABAergic neurons in the nucleus of the optic tract project to the superior colliculus: an ultrastructural retrograde tracer and immunocytochemical study in the rabbit. J. Comp. Neurol., 350, 646-656.
45. Nunes Cardozo, B., & Wortel, J. (1993) Projections from and to the superior colliculus in the nucleus of the optic tract combined with postembedding GABA immunocytochemistry in the rabbit. Eur. J. Morph., 31, 92-96.
46. Pong, M. & Fuchs, A.F. (2000) Characteristics of the pupillary light reflex in the macaque monkey: discharge patterns of pretectal neurons. J. Neurophysiol., 84, 964-974.
47. Schiff, D., Cohen, B., Buttner-Ennever, J. & Matsuo, V. (1990) Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and afternystagmus in the monkey. Exp. Brain Res., 79, 225-239.
48. Schmidt, M. (1996) Neurons in the cat pretectum that project to the dorsal lateral geniculate nucleus are activated during saccades. J. Neurophysiol., 76, 2907-2918.
49. Schmidt, M., Boller, M., Özen, G. & Hall, W.C. (2001a) Disinhibition in rat superior colliculus mediated by GABAc receptors. J. Neurosci., 21, 691-699.
50. Schmidt, M. & Hoffmann, K.P. (1992) Physiological identification of pretectal neurons projecting to the lateral geniculate nucleus in the cat. Eur. J. Neurosci., 4, 318-326.
51. Schmidt, M., Sudkamp, S. & Wahle, P. (2001b) Characterization of pretectal-nuclear-complex afferents to the pulvinar in the cat. Exp. Brain Res., 138, 509-519.
52. Schweigart, G. & Hoffmann, K.P. (1992) Pretectal jerk neuron activity during saccadic eye movements and visual stimulations in the cat. Exp. Brain Res., 91, 273-283.
53. Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988) The pretectal nuclear complex. In Büttner-Ennever, J. (ed.), Neuroanatomy of the Oculomotor System. Elsevier, Amsterdam, p. 335.
54. Sparks, D.L. (1986) Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol. Rev., 66, 118-171.
55. Sudkamp, S. & Schmidt, M. (1995) Physiological characterization of pretectal neurons projecting to the lateral posterior-pulvinar complex in the cat. Eur. J. Neurosci., 1, 881-888.
56. Van der Want, J.J., Nunes Cardozo, J. & van der Togt, C. (1992) GABAergic neurons and circuits in the pretectal nuclei and the accessory optic system of mammals. Prog. Brain Res., 90, 283-305.
57. Wahle, P., Stuphorn, V., Schmidt, M. & Hoffmann, K.P. (1994) LGN-projecting neurons in the cat's pretectum express glutamic acid decarboxylase mRNA. Eur. J. Neurosci., 6, 454-460.
58. Wang, S. & Bickford, M.E. (2000) Anatomical characterization of the projection from the pretectum to the pulvinar nucleus of the cat. Soc. Neurosci. Abstr., 26, 1470.
59. Wang, S., Eisenback, M.A., Datskovskaia, A., Boyce, M.J. & Bickford, M.E. (2002) GABAergic pretectal terminals contact GABAergic interneurons in the cat dorsal lateral geniculate nucleus. Neurosci. Lett., 323, 141-145.