Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T12:49:09.638Z Has data issue: false hasContentIssue false
  • English
  • Français

Afferent connectivity to different functional zones of the optic tectum in goldfish

Published online by Cambridge University Press:  18 November 2003

M.P. PÉREZ-PÉREZ ,
M.A. LUQUE ,
L. HERRERO ,
P.A. NÚÑEZ-ABADES  and
B. TORRES
M.P. PÉREZ-PÉREZ
Affiliation:
Lab. Neurobiología de Vertebrados, Dept. Fisiología y Zoología, Univ. Sevilla, Spain
M.A. LUQUE
Affiliation:
Lab. Neurobiología de Vertebrados, Dept. Fisiología y Zoología, Univ. Sevilla, Spain
L. HERRERO
Affiliation:
Lab. Neurobiología de Vertebrados, Dept. Fisiología y Zoología, Univ. Sevilla, Spain
P.A. NÚÑEZ-ABADES
Affiliation:
Lab. Neurobiología de Vertebrados, Dept. Fisiología y Zoología, Univ. Sevilla, Spain
B. TORRES
Affiliation:
Lab. Neurobiología de Vertebrados, Dept. Fisiología y Zoología, Univ. Sevilla, Spain
Get access Rights & Permissions [Opens in a new window]

Abstract

This work studies the afferent connectivity to different functionally identified tectal zones in goldfish. The sources of afferents contributed to different degrees to the functionally defined zones. The dorsocentral area of the telencephalon was connected mainly with the ipsilateral anteromedial tectal zone. At diencephalic levels, neurons were found in three different regions: preoptic, thalamic, and pretectal. Preoptic structures (suprachiasmatic and preoptic nuclei) projected mainly to the anteromedial tectal zone, whereas thalamic (ventral and dorsal) and pretectal (central, superficial, and posterior commissure) nuclei projected to all divisions of the tectum. In the mesencephalon, the mesencephalic reticular formation, torus longitudinalis, torus semicircularis, and nucleus isthmi were, in the anteroposterior axis, topographically connected with the tectum. In addition, neurons in the contralateral tectum projected to the injected zones in a symmetrical point-to-point correspondence. At rhombencephalic levels, the superior reticular formation was connected to all studied tectal zones, whereas medial and inferior reticular formations were connected with medial and posterior tectal zones. The present results support a different quantitative afferent connectivity to each tectal zone, possibly based on the sensorimotor transformations that the optic tectum carries out to generate orienting responses.

Keywords

Optic tectumTectal afferentsEye movementsGoldfishTeleost
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 4 , July 2003 , pp. 397 - 410
Copyright
2003 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

REFERENCES

Akert, K. (1949). Der visualle greireflex. Helvetica Physiologica Pharmacologica Acta 7, 112–134.Google Scholar
Al-Akel, A.S., Guthrie, D.M., & Banks, J.R. (1986). Motor responses to localized electrical stimulation of the tectum in the freshwater perch (Perca fluviatilis). Neuroscience 19, 1381–1391.Google Scholar
Appell, P.P. & Behan, M. (1990). Sources of subcortical GABAergic projections to the superior colliculus in the cat. Journal of Comparative Neurology 302, 143–158.Google Scholar
Bernau, N.A., Puzdrowski, R.L., & Leonard, R.B. (1991). Identification of the midbrain locomotor region and its relation to descending locomotor pathways in the Atlantic stingray, Dasyatis sabina. Brain Research 557, 83–94.Google Scholar
Büttner-Ennever, J.A. & Büttner, U. (1978). A cell group associated with vertical eye movements in the rostral mesencephalic reticular formation of the monkey. Brain Research 151, 31–47.Google Scholar
Chen, B. & May, P.J. (2000). The feedback circuit connecting the superior colliculus and central mesencephalic reticular formation: A direct morphological demonstration. Experimental Brain Research 131, 10–21.Google Scholar
Cohen, B., Matsuo, V., Fradin, J., & Raphan, T. (1985). Horizontal saccades induced by stimulation of the central mesencephalic reticular formation. Experimental Brain Research 57, 605–616.Google Scholar
Correa, S.A., Grant, K., & Hofmann, A. (1998). Afferent and efferent connections of the dorsocentral telencephalon in an electrosensory teleost, Gymnotus carapo. Brain, Behavior, and Evolution 52, 81–98.Google Scholar
Dacey, D.M. & Ulinski, P.S. (1986). Optic tectum of the eastern garter snake, Thamnophis sirtalis. I. Efferent pathways. Journal of Comparative Neurology 245, 1–28.Google Scholar
Demski, L.S. (1982). Eye movements and related behavioral responses evoked by electrical stimulation of the brain in free-swimming sunfish. Brain, Behavior, and Evolution 20, 182–195.Google Scholar
Demski, L.S. (1983). Behavioral effects of electrical stimulation of the brain. In Fish Neurobiology. Higher Brain Areas and Functions, ed. Davis, R.E. & Northcutt, R.G., pp. 317–359. Ann Arbor, Michigan: The University of Michigan Press.
Dunn-Meynell, A.A. & Sharma, S.C. (1984). Changes in the topographically organized connections between the nucleus isthmi and the optic tectum after partial tectal ablation in adult goldfish. Journal of Comparative Neurology 227, 497–510.Google Scholar
Edwards, S.B., Ginsburg, C.L., Henkel, C.K., & Stein, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.Google Scholar
Ewert, J.P. (1984). Tectal mechanisms that underlie prey-catching and avoidance behaviors in toads. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 247–416. New York: Plenum Press.
Fetcho, J.R. & Svoboda, K.R. (1993). Fictive swimming elicited by electrical stimulation of the midbrain in goldfish. Journal of Neurophysiology 70, 765–780.Google Scholar
Fiebig, E., Ebbesson, S.O.E., & Meyer, D.L. (1983). Afferent connections of the optic tectum in the piranha (Serrasalmus nattereri). Cell Tissue Research 231, 55–72.Google Scholar
Fukushima, K. (1987). The interstitial nucleus of Cajal and its role in the control of movements of the head and eyes. Progress in Neurobiology 29, 107–192.Google Scholar
Gestring, P. & Sterling, P. (1977). Anatomy and physiology of goldfish oculomotor system. II. Firing patterns of neurons in abducens nucleus and surrounding medulla and their relation to eye movements. Journal of Neurophysiology 40, 573–588.Google Scholar
Gibbs, M.A. & Northmore, D.P.M. (1996). The role of torus longitudinalis in equilibrium orientation measured with the dorsal light reflex. Brain, Behavior, and Evolution 48, 115–120.Google Scholar
Gibbs, M.A. & Northmore, D.P.M. (1998). Spectral sensitivity of the goldfish, Torus longitudinalis. Visual Neuroscience 15, 859–865.Google Scholar
Grofova, O., Ottersen, O.P., & Rinvik, E. (1978). Mesencephalic and diencephalic afferents to the superior colliculus and periaqueductal gray substance demonstrated by retrograde axonal transport of horseradish peroxidase in the cat. Brain Research 146, 205–220.Google Scholar
Grover, B.G. & Sharma, S.C. (1979). Tectal projections in the goldfish (Carassius auratus): A degeneration study. Journal of Comparative Neurology 184, 435–454.Google Scholar
Grover, B.G. & Sharma, S.C. (1981). Organization of extrinsic tectal connections in goldfish (Carassius auratus). Journal of Comparative Neurology 196, 471–488.Google Scholar
Guitton, D., Crommelinck, M., & Roucoux, A. (1980). Stimulation of the superior colliculus in the alert cat. I. Eye movements and neck EMG activity evoked when the head is restrained. Experimental Brain Research 39, 63–73.Google Scholar
Güntürkün, O. & Remy, M. (1990). The topographical projection of the nucleus isthmi pars parvocellularis (Ipc) onto the tectum opticum in the pigeon. Neuroscience Letters 111, 18–22.Google Scholar
Herrero, L., Corvisier, J., Hardy, O., & Torres, B. (1998a). Influence of the tectal zone on the distribution of synaptic boutons in the brainstem of goldfish. Journal of Comparative Neurology 401, 411–428.Google Scholar
Herrero, L., Rodriguez, F., Salas, C., & Torres, B. (1998b). Tail and eye movements evoked by electrical microstimulation from the optic tectum in goldfish. Experimental Brain Research 120, 291–305.Google Scholar
Herrero, L., Pérez, P., Núñez-Abades, P.A., Hardy, O., & Torres, B. (1999). Tectotectal connectivity in goldfish. Journal of Comparative Neurology 411, 455–471.Google Scholar
Hofmann, M.H., Ebbesson, S.O.E., & Meyer, D.L. (1990). Tectal afferents in Rana pipiens. A reassessment questioning the comparability of HRP results. Journal für Hirnforschung 31, 337–340.Google Scholar
Ito, H. & Kishida, R. (1977). Tectal afferent neurons identified by the retrograde HRP method in the carp telencephalon. Brain Research 130, 142–145.Google Scholar
Ito, H., Kishida, R. (1978). Afferent and efferent fiber connections of the carp torus longitudinalis. Journal of Comparative Neurology 181, 465–475.Google Scholar
Ito, H., Tanaka, H., Sakamoto, N., & Morita, Y. (1981). Isthmic afferent neurons identified by the retrograde HRP method in a teleost, Navodon modestus. Brain Research 207, 163–169.Google Scholar
Ito, H., Sakamoto, N., & Takatsuji, K. (1982). Cytoarchitecture, fiber connections, and ultrastructure of nucleus isthmi in a teleost (Navodon modestus) with a special reference to degenerating isthmic afferents from optic tectum and nucleus pretectalis. Journal of Comparative Neurology 205, 299–311.Google Scholar
Jiang, Z.D., Moore, D.R., & King, A.J. (1997). Sources of subcortical projections to the superior colliculus in the ferret. Brain Research 755, 279–292.Google Scholar
Knudsen, E.I. & Brainard, M.S. (1995). Creating a unified representation of visual and auditory space in the brain. Annuals of Review Neuroscience 18, 19–43.Google Scholar
Knudsen, E.I., Cohen, Y.E., & Masino, T. (1995). Characterization of a forebrain gaze field in the archistriatum of the barn owl: Microstimulation and anatomical connections. Journal of Neuroscience 15, 5139–5151.Google Scholar
Kunzle, H., Schnyder, N. (1984). The isthmus-tegmentum complex in the turtle and rat: A comparative analysis of its interconnections with the optic tectum. Experimental Brain Research 56, 509–522.Google Scholar
Lee, L.T. & Bullock, T.H. (1990). Responses of the optic tectum to telencephalic stimulation in catfish. Brain, Behavior, and Evolution 35, 313–324.Google Scholar
Leichnetz, G.R. & Gonzalo-Ruiz, A. (1987). Collaterization of frontal eye field (medial precentral/anterior cingulate) neurons projecting to the paraoculomotor region, superior colliculus, and medial pontine reticular formation in the rat: A fluorescent double-labeling study. Experimental Brain Research 68, 355–364.Google Scholar
Lu, Z. & Fay, R.R. (1993). Acoustic response properties of single units in the torus semicircularis of the goldfish, Carassius auratus. Journal of Comparative Physiology 173, 33–48.Google Scholar
Luiten, P.G.M. (1981). Afferent and efferent connections of the optic tectum in the carp (Cyprinus carpio L.). Brain Research 220, 51–65.Google Scholar
Masino, T. & Knudsen, E.I. (1993). Orienting head movements resulting from electrical microstimulation of the brainstem tegmentum in the barn owl. Journal of Neuroscience 13, 351–370.Google Scholar
Meek, J. & Nieuwenhuys, R. (1998). Holosteans and teleosteans. In The Central Nervous System of Vertebrates, ed. Nieuwenhuys, R., Ten Donkelaar, H.J. & Nicholson, C., pp. 760–937. Berlin–Heidelberg–New York–Tokyo: Springer-Verlag.
Meyer, D.L., Schott, D., & Schaefer, K.P. (1970). Reizversuche im tectum opticum freischwimmeder abeljaue bzw. Dorsche (Gadus morrhua L.). Pflügers Archive 314, 240–252.Google Scholar
Moschovakis, A.K. & Highstein, S.M. (1994). The anatomy and physiology of primate neurons that control rapid eye movements. Annuals Review of Neuroscience 17, 465–488.Google Scholar
Moschovakis, A.K., Kitama, T., Dalezios, Y., Petit, J., Brandi, A.M., & Grantyn, A.A. (1998). An anatomical substrate for the spatiotemporal transformation. Journal of Neuroscience 18, 10219–10229.Google Scholar
Niida, A. & Ohono, T. (1984). An extensive projection of fish dorsolateral tegmental cells to the optic tectum revealed by intra axonal dye marking. Neuroscience Letters 48, 261–266.Google Scholar
Northcutt, R.G. (1982). Localization of neurons afferent to the optic tectum in longnose gars. Journal of Comparative Neurology 204, 325–335.Google Scholar
Northcutt, R.G. & Butler, A.B. (1980). Projections of the optic tectum in the longnose gar, Lepisosteus osseus. Brain Research 190, 333–346.Google Scholar
Northmore, D.P.M. (1984). Visual and saccadic activity in the goldfish torus longitudinalis. Journal of Comparative Physiology 15, 333–340.Google Scholar
Northmore, D.P.M. (1991). Visual responses of nucleus isthmi in a teleost fish (Lepomis macrochirus). Vision Research 31, 525–535.Google Scholar
Northmore, D.P.M., Williams, B., & Vanegas, H. (1983). The teleostean torus longitudinalis: Responses related to eye movements; visuotopic mapping, and functional relationships with the optic tectum. Journal of Comparative Physiology 150, 39–50.Google Scholar
Perez-Perez, M.P., Herrero, L., & Torres, B. (2000). Connectivity of the tectal zones coding for upward and downward oblique eye movements in goldfish. Journal of Comparative Neurology 427, 405–416.Google Scholar
Rettig, G. (1988). Connections of the tectum opticum in two urodeles, Salamandra salamandra and Bolitoglossa subpalmata, with special reference to the nucleus isthmi. Journal für Hirnforschung 29, 5–16.Google Scholar
Robinson, D.A. (1972). Eye movements evoked by collicular stimulation in the alert monkey. Vision Research 12, 1795–1808.Google Scholar
Sakamoto, N., Ito, H., & Ueda, S. (1981). Topographic projections between the nucleus isthmi and the optic tectum in a teleost. Navodon modestus. Brain Research 224, 225–234.Google Scholar
Salas, C., Navarro, F., Torres, B., & Delgado-García, J.M. (1992). Effects of diazepam and D-amphetamine on rhythmic pattern of eye movements in goldfish. Neuroreport 3, 131–134.Google Scholar
Salas, C., Herrero, L., Rodríguez, F., & Torres, B. (1997). Tectal codification of eye movements in goldfish studied by electrical microstimulation. Neuroscience 78, 271–288.Google Scholar
Schlussman, S.D., Kobylack, M.A., Dunn-Meynell, A.A., & Sharma, S.C. (1990). Afferent connections of the optic tectum in channel catfish, Ictalurus punctatus. Cell Tissue Research 262, 531–541.Google Scholar
Smeets, W.J. (1982). The afferent connections of the tectum mesencephali in two chondrichthyans, the shark Scyliorhinus canicula and the ray Raja clavata. Journal of Comparative Neurology 205, 139–152.Google Scholar
Sparks, D.L. & Mays, L.E. (1989). Signal transformations required for the generation of saccadic eye movements. Annuals Review of Neuroscience 13, 309–336.Google Scholar
Stanton, G.B., Goldberg, M.E., & Bruce, C.J. (1988). Frontal eye field efferents in the macaque monkey. II. Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.Google Scholar
Stein, B.E. (1998). Neural mechanisms for synthesizing sensory information and producing adaptive behaviors. Experimental Brain Research 123, 124–135.Google Scholar
Stein, B.E. & Gaither, N.S. (1981). Sensory representation in reptilian optic tectum: Some comparisons with mammals. Journal of Comparative Neurology 202, 69–87.Google Scholar
Taylor, A.M., Jeffery, G., & Lieberman, A.R. (1986). Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains. Experimental Brain Research 62, 131–142.Google Scholar
ten Donkelaar, H.J. (1998). Reptiles. In The Central Nervous System of Vertebrates, ed. Nieuwenhuys, R., ten Donkelaar, H.J. & Nicholson, C., pp. 1315–1524. Berlin, Heidelberg, New York, Tokyo: Springer-Verlag.
Torres, B., Pastor, A.M., Cabrera, B., Salas, C., & Delgado-García, J.M. (1992). Afferents to the oculomotor nucleus in the goldfish (Carassius auratus) as revealed by retrograde labeling with horseradish peroxidase. Journal of Comparative Neurology 324, 449–461.Google Scholar
Torres, B., Fernandez, S., Rodríguez, F., & Salas, C. (1995). Distribution of neurons projecting to the trochlear nucleus in goldfish (Carassius auratus). Brain, Behavior, and Evolution 45, 272–285.Google Scholar
Tóth, P., Lazar, G., Wang, S.R., Li, T.B., Xu, J., Pal, E., & Straznicky, C. (1994). The contralaterally projecting neurons of the isthmic nucleus in five anuran species: A retrograde tracing study with HRP and cobalt. Journal of Comparative Neurology 346, 306–320.Google Scholar
Uematsu, K. & Todo, T. (1997). Identification of the midbrain locomotor nuclei and their descending pathways in the teleost carp, Cyprinus carpio. Brain Research 773, 1–7.Google Scholar
Vanegas, H. (1984). Comparative Neurology of the Optic Tectum. New York: Plenum Press.
Waitzman, D.M., Silakov, V.L., DePalma, S., & Ayers, A.S. (2000a). Effects of reversible inactivation of the primate mesencephalic reticular formation. I. Hypermetric goal-directed saccades. Journal of Neurophysiology 83, 2260–2284.Google Scholar
Waitzman, D.M., Silakov, V.L., DePalma, S., & Ayers, A.S. (2000b). Effects of reversible inactivation of the primate mesencephalic reticular formation. II. Hypometric vertical saccades. Journal of Neurophysiology 83, 2285–2289.Google Scholar
Wilczyniski, W. & Northcutt, R.G. (1977). Afferents to the optic tectum of the leopard frog: an HRP study. Journal of Comparative Neurology 173, 219–230.Google Scholar
Wubbels, R.J. & Schellart, N.A. (1997). Neuronal encoding of sound direction in the auditory midbrain of the rainbow trout. Journal of Neurophysiology 77, 3060–3074.Google Scholar
Wulliman, M.F. (1994). The teleostean torus longitudinalis: A short review on its structure, histochemistry, connectivity, possible function and phylogeny. European Journal of Morphology 32, 235–242.Google Scholar
Yamane, Y., Yoshimoto, M., & Ito, H. (1996). Area dorsalis pars lateralis of the telencephalon in a teleost (Sebasticus marmoratus) can be divided into dorsal and ventral regions. Brain, Behavior, and Evolution 48, 338–349.Google Scholar
Zittlau, K.E., Claas, B., & Münz, H. (1988). Horseradish peroxidase study of tectal afferents in Xenopus laevis with special emphasis on their relationship to the lateral-line system. Brain, Behavior, and Evolution 32, 208–219.Google Scholar