Afferent and efferent connections of the nucleus prethalamicus in the yellowfin goby Acanthogobius flavimanus.
acanthopterygian fish
cerebellum
nucleus prethalamicus
optic tectum
telencephalon
teleosts
visual pathway
Journal
The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041
Informations de publication
Date de publication:
01 2021
01 2021
Historique:
received:
18
10
2018
revised:
19
04
2020
accepted:
20
04
2020
pubmed:
28
4
2020
medline:
17
12
2021
entrez:
28
4
2020
Statut:
ppublish
Résumé
The nucleus prethalamicus (PTh) receives fibers from the optic tectum and then projects to the dorsal telencephalon in the yellowfin goby Acanthogobius flavimanus. However, it remained unclear whether the PTh is a visual relay nucleus, because the optic tectum receives not only visual but also other sensory modalities. Furthermore, precise telencephalic regions receiving prethalamic input remained unknown in the goby. We therefore investigated the full set of afferent and efferent connections of the PTh by direct tracer injections into the nucleus. Injections into the PTh labeled cells in the optic tectum, ventromedial thalamic nucleus, central and medial parts of the dorsal telencephalon, and caudal lobe of the cerebellum. We found that the somata of most tecto-prethalamic neurons are present in the stratum periventriculare. Their dendrites ascend to reach the major retinorecipient layers of the tectum. The PTh is composed of two subnuclei (medial and lateral) and topographic organization was appreciated only for tectal projections to the lateral subnucleus (PTh-l), which also receives sparse retinal projections. In contrast, the medial subnucleus receives fibers only from the medial tectum. We found that the PTh projects to nine subregions in the dorsal telencephalon and four in the ventral telencephalon. Furthermore, cerebellar injections revealed that cerebello-prethalamic fibers cross the midline twice to innervate the PTh-l on both sides. The present study is the first detailed report on the full set of the connections of PTh, which suggests that the PTh relays visual information from the optic tectum to the telencephalon.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
87-110Informations de copyright
© 2020 Wiley Periodicals, Inc.
Références
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 Research, 173, 1-11. https://doi.org/10.1016/0006-8993(79)91090-4
Baldwin, M. K. L., Balaram, P., & Kaas, J. H. (2017). The evolution and functions of nuclei of the visual pulvinar in primates. The Journal of Comparative Neurology, 525, 3207-3226. https://doi.org/10.1002/cne.24272
Benevento, L. A., & Fallon, J. H. (1975). The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). The Journal of Comparative Neurology, 160, 339-361. https://doi.org/10.1002/cne.901600306
Ben-Tov, M., Kopilevich, I., Donchin, O., Ben-Shahar, O., Giladi, C., & Segev, R. (2013). Visual receptive field properties of cells in the optic tectum of the archer fish. Journal of Neurophysiology, 110, 748-759. https://doi.org/10.1152/jn.00094.2013
Boire, D., Matteau, I., Casanova, C., & Ptito, M. (2004). Retinal projections to the lateral posterior-pulvinar complex in intact and early visual cortex lesioned cats. Experimental Brain Research, 159, 185-196. https://doi.org/10.1007/s00221-004-1946-6
Braford, M. R., Jr., & Northcutt, R. G. (1983). Organization of the diencephalon and pretectum of the ray-finned fishes. In R. E. Davis & R. G. Northcutt (Eds.), Fish neurobiology (Vol. 2, pp. 117-163). Ann Arbor, MI: The University of Michigan Press.
Butler, A. B. (1978). Organization of ascending tectal projections in the lizard Gekko gecko: A new pattern of tectorotundal inputs. Brain Research, 147, 353-361. https://doi.org/10.1016/0006-8993(78)90845-4
Campbell, C. B. G., & Ebbesson, S. O. E. (1969). The optic system of a teleost: Holocentrus re-examined. Brain, Behavior and Evolution, 2, 415-430. https://doi.org/10.1159/000125898
Chomsung, R. D., Petry, H. M., & Bickford, M. E. (2008). Ultrastructural examination of diffuse and specific tectopulvinar projections in the tree shrew. The Journal of Comparative Neurology, 510, 24-46. https://doi.org/10.1002/cne.21763
Cynader, M., & Berman, N. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology, 35, 187-201. https://doi.org/10.1152/jn.1972.35.2.187
Day-Brown, J. D., Wei, H., Chomsung, R. D., Petry, H. M., & Bickford, M. E. (2010). Pulvinar projections to the striatum and amygdala in the tree shrew. Frontiers in Neuroanatomy, 4, 143. https://doi.org/10.3389/fnana.2010.00143
Ebbesson, S. O. E. (1980). A visual thalamo-telencephalic pathway in a teleost fish (Holocentrus rufus). Cell and Tissue Research, 213, 505-508. https://doi.org/10.1007/BF00237895
Ebbesson, S. O. E., & Vanegas, H. (1976). Projections of the optic tectum in two teleost species. The Journal of Comparative Neurology, 165, 161-180. https://doi.org/10.1002/cne.901650204
Elliott, S. B., Harvey-Girard, E., Giassi, A. C. C., & Maler, L. (2017). Hippocampal-like circuitry in the pallium of an electric fish: Possible substrates for recursive pattern separation and completion. The Journal of Comparative Neurology, 525, 8-46. https://doi.org/10.1002/cne.24060
Finger, T. E. (1978). Efferent neurons of the teleost cerebellum. Brain Research, 153, 608-614. https://doi.org/10.1016/0006-8993(78)90346-3
Finger, T. E. (2000). Ascending spinal systems in the fish, Prionotus carolinus. The Journal of Comparative Neurology, 422, 106-122. https://doi.org/10.1002/(SICI)1096-9861(20000619)422:1<106::AID-CNE7>3.0.CO;2-T
Finger, T. E., & Tong, S. L. (1984). Central organization of eighth nerve and mechanosensory lateral line systems in the brainstem of ictalurid catfish. The Journal of Comparative Neurology, 229, 129-151. https://doi.org/10.1002/cne.902290110
Folgueira, M., Anadón, R., & Yáñez, J. (2004). Experimental study of the connections of the telencephalon in the rainbow trout (Oncorhynchus mykiss). II: Dorsal area and preoptic region. The Journal of Comparative Neurology, 480, 204-233. https://doi.org/10.1002/cne.20341
Folgueira, M., Anadón, R., & Yáñez, J. (2005). Experimental study of the connections of the preglomerular nuclei and corpus mamillare in the rainbow trout, Oncorhynchus mykiss. Brain Research Bulletin, 66, 361-364. https://doi.org/10.1016/j.brainresbull.2005.03.001
Folgueira, M., Anadón, R., & Yáñez, J. (2006). Afferent and efferent connections of the cerebellum of a salmonid, the rainbow trout (Oncorhynchus mykiss): A tract-tracing study. The Journal of Comparative Neurology, 497, 542-565. https://doi.org/10.1002/cne.20979
Fredes, F., Vega-Zuniga, T., Karten, H., & Mpodozis, J. (2012). Bilateral and ipsilateral ascending tectopulvinar pathways in mammals: A study in the squirrel (Spermophilus beecheyi). The Journal of Comparative Neurology, 520, 1800-1818. https://doi.org/10.1002/cne.23014
Furlan, G., Cuccioli, V., Vuillemin, N., Dirian, L., Muntasell, A. J., Coolen, M., … Bally-Cuif, L. (2017). Life-long neurogenic activity of individual neural stem cells and continuous growth establish an outside-in architecture in the teleost pallium. Current Biology, 27, 3288-3301. https://doi.org/10.1016/j.cub.2017.09.052
Giassi, A. C. C., Duarte, T. T., Ellis, W., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: II. Extrinsic connections. The Journal of Comparative Neurology, 520, 3338-3368. https://doi.org/10.1002/cne.23109
Giassi, A. C. C., Harvey-Girard, E., Valsamis, B., & Maler, L. (2012). Organization of the gymnotiform fish pallium in relation to learning and memory: I. Cytoarchitectonics and cellular morphology. The Journal of Comparative Neurology, 520, 3314-3337. https://doi.org/10.1002/cne.23097
Graham, J., & Casagrande, V. A. (1980). A light microscopic and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). The Journal of Comparative Neurology, 191, 133-151. https://doi.org/10.1002/cne.901910108
Hagio, H., Sato, M., & Yamamoto, N. (2018). An ascending visual pathway to the dorsal telencephalon through the optic tectum and nucleus prethalamicus in the yellowfin goby Acanthogobius flavimanus (Temminck & Schlegel, 1845). The Journal of Comparative Neurology, 526, 1733-1746. https://doi.org/10.1002/cne.24444
Imura, K., Yamamoto, N., Yoshimoto, M., Endo, M., Funakoshi, K., & Ito, H. (2017). Fiber connections of the caudal corpus cerebelli, with special reference to the intrinsic circuitry, in a teleost (Oreochromis niloticus). Brain, Behavior and Evolution, 89, 15-32. https://doi.org/10.1159/000455962
Ito, H., Morita, Y., Sakamoto, N., & Ueda, S. (1980). Possibility of telencephalic visual projection in teleosts, Holocentridae. Brain Research, 197, 219-222. https://doi.org/10.1016/0006-8993(80)90448-5
Ito, H., & Vanegas, H. (1983). Cytoarchitecture and ultrastructure of nucleus prethalamicus, with special reference to degenerating afferents from optic tectum and telencephalon, in a teleost (Holocentrus ascensionis). The Journal of Comparative Neurology, 221, 401-415. https://doi.org/10.1002/cne.902210404
Ito, H., & Vanegas, H. (1984). Visual receptive thalamopetal neurons in the optic tectum of teleosts (Holocentridae). Brain Research, 290, 201-210. https://doi.org/10.1016/0006-8993(84)90938-7
Itoh, K., Mizuno, N., & Kudo, M. (1983). Direct retinal projections to the lateroposterior and pulvinar nuclear complex (LP-Pul) in the cat, as revealed by the anterograde HRP method. Brain Research, 276, 325-328. https://doi.org/10.1016/0006-8993(83)90740-0
Itoh, K., Mizuno, N., Sugimoto, T., Nomura, S., Nakamura, Y., & Konishi, A. (1979). A cerebello-pulvino-cortical and a retino-pulvino-cortical pathways in the cat as revealed by the use of the anterograde and retrograde transport of horseradish peroxidase. The Journal of Comparative Neurology, 187, 349-357. https://doi.org/10.1002/cne.901870206
Kaas, J. H., Huerta, M. F., Weber, J. T., & Harting, J. K. (1978). Patterns of retinal terminations and laminar organization of the lateral geniculate nucleus of primates. The Journal of Comparative Neurology, 182, 517-553. https://doi.org/10.1002/cne.901820308
Kage, T., Takeda, H., Yasuda, T., Maruyama, K., Yamamoto, N., Yoshimoto, M., … Ishikawa, Y. (2004). Morphogenesis and regionalization of the medaka embryonic brain. The Journal of Comparative Neurology, 476, 219-239. https://doi.org/10.1002/cne.20219
Kawaguchi, M., Hagio, H., Yamamoto, N., Matsumoto, K., Nakayama, K., Akazome, Y., … Ichijo, H. (2019). Atlas of the telencephalon based on cytoarchitecture, neurochemical markers, and gene expressions in Rhinogobius flumineus (Mizuno, 1960). The Journal of Comparative Neurology, 527, 874-900. https://doi.org/10.1002/cne.24547
Kinoshita, M., Ito, E., Urano, A., Ito, H., & Yamamoto, N. (2006). Periventricular efferent neurons in the optic tectum of rainbow trout. The Journal of Comparative Neurology, 499, 546-564. https://doi.org/10.1002/cne.21080
Lee, L. T., & Bullock, T. H. (1984). Sensory representation in the cerebellum of the catfish. Neuroscience, 13, 157-169. https://doi.org/10.1016/0306-4522(84)90266-5
Luppino, G., Matelli, M., Carey, R. G., Fitzpatrick, D., & Diamond, I. T. (1988). New view of the organization of the pulvinar nucleus in Tupaia as revealed by tectopulvinar and pulvinar-cortical projections. The Journal of Comparative Neurology, 273, 67-86. https://doi.org/10.1002/cne.902730107
Marín, G., Letelier, J. C., Henny, P., Sentis, E., Farfán, G., Fredes, F., … Mpodozis, J. (2003). Spatial organization of the pigeon tectorotundal pathway: An interdigitating topographic arrangement. The Journal of Comparative Neurology, 458, 361-380. https://doi.org/10.1002/cne.10591
McCormick, C. A., & Hernandez, D. V. (1996). Connections of octaval and lateral line nuclei of the medulla in the goldfish, including the cytoarchitecture of the secondary octaval population in goldfish and catfish. Brain, Behavior and Evolution, 47, 113-137. https://doi.org/10.1159/000113232
Meader, R. G. (1934). The optic system of the teleost, Holocentrus. I. The primary optic pathways and the corpus geniculatum complex. The Journal of Comparative Neurology, 60, 361-407. https://doi.org/10.1002/cne.900600303
Meek, J., & Schellart, N. A. M. (1978). A Golgi study of goldfish optic tectum. The Journal of Comparative Neurology, 182, 89-122. https://doi.org/10.1002/cne.901820107
Miyazaki, T., Kato, A., Ikenaga, T., Hagio, H., & Yamamoto, N. (2019). A lambda-shaped retractor lentis muscle in the yellowfin goby Acanthogobius flavimanus. Journal of Morphology, 280, 526-533. https://doi.org/10.1002/jmor.20961
Murakami, T., & Morita, Y. (1987). Morphology and distribution of the projection neurons in the cerebellum in a teleost, Sebastiscus marmoratus. The Journal of Comparative Neurology, 256, 607-623. https://doi.org/10.1002/cne.902560413
Murakami, T., Morita, Y., & Ito, H. (1983). Extrinsic and intrinsic fiber connections of the telencephalon in a teleost, Sebastiscus marmoratus. The Journal of Comparative Neurology, 216, 115-131. https://doi.org/10.1002/cne.902160202
Nelson, J. S., Grande, T. C., & Wilson, M. V. H. (2016). Fishes of the world (fifth ed.). Hoboken, NJ: John Wiley & Sons, Inc. https://doi.org/10.1002/9781119174844
Nieuwenhuys, R. (1963). The comparative anatomy of the actinopterygian forebrain. Journal für Hirnforschung, 7, 171-192.
Northcutt, R. G. (2006). Connections of the lateral and medial divisions of the goldfish telencephalic pallium. The Journal of Comparative Neurology, 494, 903-943. https://doi.org/10.1002/cne.20853
Ou, R., & Yamamoto, N. (2016). Forebrain atlas of Japanese jack mackerel Trachurus japonicus. Ichthyological Research, 63, 405-426. https://doi.org/10.1007/s10228-016-0509-8
Partlow, G. D., Colonnier, M., & Szabo, J. (1977). Thalamic projections of the superior colliculus in the rhesus monkey, Macaca mulatta. A light and electron microscopic study. The Journal of Comparative Neurology, 171, 285-317. https://doi.org/10.1002/cne.901710302
Petry, H. M., & Bickford, M. E. (2019). The second visual system of the tree shrew. The Journal of Comparative Neurology, 527, 679-693. https://doi.org/10.1002/cne.24413
Rainey, W. T., & Ulinski, P. S. (1982). Organization of nucleus rotundus, a tectofugal thalamic nucleus in turtles. III. The tectorotundal projection. The Journal of Comparative Neurology, 209, 208-223. https://doi.org/10.1002/cne.902090207
Robson, J. A., & Hall, W. C. (1977). The organization of the pulvinar in the grey squirrel (Sciurus carolinensis). I. Cytoarchitecture and connections. The Journal of Comparative Neurology, 173, 355-388. https://doi.org/10.1002/cne.901730210
Rodrigo-Angulo, M. L., & Reinoso-Suarez, F. (1984). Cerebellar projections to the lateral posterior-pulvinar thalamic complex in the cat. Brain Research, 322, 172-176. https://doi.org/10.1016/0006-8993(84)91200-9
Schneider, G. E. (1969). Two visual systems. Science, 163, 895-902. https://doi.org/10.1126/science.163.3870.895
Schwassmann, H. O., & Kruger, L. (1965). Organization of the visual projection upon the optic tectum of some freshwater fish. The Journal of Comparative Neurology, 124, 113-126. https://doi.org/10.1002/cne.901240109
Stepniewska, I., Qi, H. X., & Kaas, J. H. (2000). Projections of the superior colliculus to subdivisions of the inferior pulvinar in New World and Old World monkeys. Visual Neuroscience, 17, 529-549. https://doi.org/10.1017/S0952523800174048
Vanegas, H., & Ito, H. (1983). Morphological aspects of the teleostean visual system: A review. Brain Research Reviews, 6, 117-137. https://doi.org/10.1016/0165-0173(83)90036-X
Wallach, A., Harvey-Girard, E., Jun, J. J., Longtin, A., & Maler, L. (2018). A time-stamp mechanism may provide temporal information necessary for egocentric to allocentric spatial transformations. eLife, 7, e36769. https://doi.org/10.7554/eLife.36769
Wilson, M. E., & Toyne, M. J. (1970). Retino-tectal and cortico-tectal projections in Macaca mulatta. Brain Research, 24, 395-406. https://doi.org/10.1016/0006-8993(70)90181-2
Wullimann, M. F., & Mueller, T. (2004). Teleostean and mammalian forebrains contrasted: Evidence from genes to behavior. The Journal of Comparative Neurology, 475, 143-162. https://doi.org/10.1002/cne.20183
Wullimann, M. F., & Northcutt, R. G. (1988). Connections of the corpus cerebelli in the green sunfish and the common goldfish: A comparison of perciform and cypriniform teleosts. Brain, Behavior and Evolution, 32, 293-316. https://doi.org/10.1159/000116558, https://doi.org/10.1159/000316057
Xue, H. G., Yamamoto, N., Yang, C. Y., Kerem, G., Yoshimoto, M., Sawai, N., … Ozawa, H. (2006). Projections of the sensory trigeminal nucleus in a percomorph teleost, tilapia (Oreochromis niloticus). The Journal of Comparative Neurology, 495, 279-298. https://doi.org/10.1002/cne.20865
Xue, H. G., Yang, C. Y., & Ito, H. (2003). Topographical projections to the nucleus prethalamicus from the cerebellum, optic tectum, and telencephalon in holocentrid teleosts. Brain Research, 992, 146-150. https://doi.org/10.1016/j.brainres.2003.08.031
Yamamoto, N., & Ito, H. (2005). Fiber connections of the central nucleus of semicircular torus in cyprinids. The Journal of Comparative Neurology, 491, 186-211. https://doi.org/10.1002/cne.20683
Yamamoto, N., & Ito, H. (2008). Visual, lateral line, and auditory ascending pathways to the dorsal telencephalic area through the rostrolateral region of the lateral preglomerular nucleus in cyprinids. The Journal of Comparative Neurology, 508, 615-647. https://doi.org/10.1002/cne.21717
Yamamoto, N., Kato, T., Okada, Y., & Somiya, H. (2010). Somatosensory nucleus in the torus semicircularis of cyprinid teleosts. The Journal of Comparative Neurology, 518, 2475-2502. https://doi.org/10.1002/cne.22348
Yamane, Y., Yoshimoto, M., & Ito, H. (1996). Area dorsalis pars lateralis of the telencephalon in a teleost (Sebastiscus marmoratus) can be divided into dorsal and ventral regions. Brain, Behavior and Evolution, 48, 338-349. https://doi.org/10.1159/000113212