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Neuropeptide Y and enkephalin immunoreactivity in retinorecipient nuclei of the hamster pretectum and thalamus

Published online by Cambridge University Press:  02 June 2009

L.R. Morin
Affiliation:
Department of Psychiatry and Program in Neurobiology and Behavior, Stony Brook University, Stony Brook
J.H. Blanchard
Affiliation:
Department of Psychiatry and Program in Neurobiology and Behavior, Stony Brook University, Stony Brook

Abstract

This investigation was stimulated by the historical confusion concerning the identity of certain pretectal nuclei and by large differences reported between species with respect to which nuclei receive retinal innervation. Subcortical visual nuclei were studied using immunohistochemistry to identify retinal projections labeled following intraocular injection of cholera toxin, b fragment. In addition, neuropeptide Y (NPY) or enkephalin (ENK) immunoreactive cells and fibers were also evaluated in the retinorecipient pretectal and thalamic areas. The results confirm the established view that the retina directly innervates the nucleus of the optic tract (NOT), posterior (PPT) and olivary pretectal (OPT) nuclei. However, the retina also innervates the hamster medial (MPT) and anterior (APT; dorsal division) pretectal nuclei, results not previously reported in rodents. A commissural pretectal area (CPT) sparsely innervated by retina is also described. The data show for the first time that the posterior limitans nucleus (PLi) receives a moderately dense, direct retinal input. The PLi does not project to the cortex and appears to be a pretectal, rather than thalamic, nucleus. All retinal projections are bilateral, although predominantly contralateral The PLi contains a moderately dense plexus of NPY- and ENK-IR fibers and terminals. However, peptidergic fibes also traverse the APT and connect with the dorsomedial pretectum. The OPT contains ENK- and NPY-IR neurons and fibers, but is specifically identifiable by a moderately dense plexus of ENK-IR terminals. Numerous ENK-IR neurons are found in the NOT and PPT. The latter also has moderate numbers of ENK-IR fibers and terminals b few NPY-IR neurons or fibers. The MPT contains modest numbers of ENK-IR fibers. The APT has no NPY-IR neurons or terminals, but an occasional ENK-IR neuron is seen and there is sparse ENK-IR innervation Peptidergic innervation of the visual nuclei does not appear to be derived from the retina. The results show a set of retinally innervated, contiguous nuclei extending from the thalamic ventrolateral geniculate nucleus dorsomedially to the midbrain CPT. These nuclei plus the superior colliculus comprise a dorsal “visual shell” embracing a central core of caudal thalamus and rostral midbrain.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1997

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References

Bons, N., Mestre, N., Petter, A., Danger, J.M., Pelletier, G. & Vaudry, H. (1990). Localization and characterization of neuropeptide Y in the brain of Microcebus murinus (Primate, Lemurian). Journal of Comparative Neurology 298, 343361.CrossRefGoogle ScholarPubMed
Botchkina, G.I. & Morin, L.P. (1995 a). Specialized neuronal and glial contributions to development of the hamster lateral geniculate complex and circadian visual system. Journal of Neuroscience 15, 190201.CrossRefGoogle ScholarPubMed
Botchkina, G.I. & Morin, L.P. (1995 b). Organization of permanent and transient neuropeptide Y-immunoreactive neuron groups and fiber systems in the developing hamster diencephalon. Journal of Comparative Neurology 357, 573602.CrossRefGoogle ScholarPubMed
Chronwall, B.M., DiMaggio, D.A., Massari, V.J., Pickel, V.M., Ruggiero, D.A. & O'Donohue, T.L. (1985). The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15, 11591181.Google Scholar
Covenas, R., Aguirre, J.A., de Leon, M., Alonso, J.R., Narvaez, J.A., Arevalo, R. & Gonzalez-Baron, S. (1990). Distribution of neuropeptide Y-like immunoreactive cell bodies and fibers in the brain stem of the cat. Brain Research Bulletin 25, 675683.CrossRefGoogle ScholarPubMed
Crain, B.J. & Hall, W.C. (1980). The normal organization of the lateral posterior nucleus of the golden hamster. Journal of Comparative Neurology 193, 351370.CrossRefGoogle ScholarPubMed
Donoghue, J.P., Kerman, K.L. & Ebner, F.F. (1979). Evidence for two organizational plans within the somatic sensory-motor cortex of the rat. Journal of Comparative Neurology 183, 647664.Google Scholar
Dursteler, M.R., Blakemore, C. & Garey, L.J. (1979). Projections to the visual cortex in the golden hamster. Journal of Comparative Neurology 183, 185204.CrossRefGoogle Scholar
Eichler, V.B. & Moore, R.Y. (1974). The primary and accessory optic systems in the golden hamster, Mesocricetus auratus. Acta Anatomica 89, 359371.CrossRefGoogle ScholarPubMed
Finley, J.C.W., Maderdrut, J.L. & Petrusz, P. (1981). The immunocytochemical localization of enkephalin in the central nervous system of the rat. Journal of Comparative Neurology 198, 541565.CrossRefGoogle ScholarPubMed
Giolli, R.A. & Guthrie, M.D. (1969). The primary optic projections in the rabbit. An experimental degeneration study. Journal of Comparative Neurology 36, 96126.Google Scholar
Goto, M., Costa, M., Peracoli, A. & Shammah-Lagnado, S.J. (1994). Efferent connections of the deep mesencephalic nucleus: A PHA-L study in the rat. Society for Neuroscience 20, 1584.Google Scholar
Graybiel, A.M. & Illing, R.-B. (1994). Enkephalin-positive and acetyl-cholincsterase-positive patch systems in the superior colliculus have matching distributions but distinct developmental histories. Journal of Comparative Neurology 340, 297310.CrossRefGoogle ScholarPubMed
Gregory, K.M. (1985). The dendritic architecture of the visual pretectal nuclei of the rat: A study with the Golgi-Cox method. Journal of Comparative Neurology 234, 122135.Google Scholar
Guillery, R.W. (1969). The organization of synaptic interconnections in the laminae of dorsal lateral geniculate nucleus of the cat. Zeitschrift für Zellforschitng 96, 138.CrossRefGoogle ScholarPubMed
Hajdu, F., Somogyi, G.Y. & Tombol, T. (1974). Neuronal and synaptic arrangement in the lateral posterior-pulvinar complex of the thalamus in the cat. Brain Research 73, 89104.CrossRefGoogle Scholar
Hendrickson, A.E., Wagoner, N. & Cowan, W.M. (1972). An autoradiographic and electron microscopic study of retinohypothalamic connections. Zeitschrift fur Zellforschung 135, 126.Google Scholar
Hermanson, O., Hallbeck, M. & Blomqvist, A. (1995). Preproenkephalin mRNA-expressing neurones in the rat thalamus. NeuroReport 6, 833836.Google Scholar
Hsu, S.-M., Raine, L. & Fanger, H. (1981). Use of avidin-biotin-peri-oxidasc complex (ABC) in immunoperioxidase techniques: A comparison between ABC and unlabelcd antibody (PAP) procedures. Journal of Histochemistry and Cytochemistry 29, 577580.CrossRefGoogle Scholar
Hutchins, B. (1991). Evidence for a direct retinal projection to the anterior pretectal nucleus in the cat. Brain Research 561, 169173.CrossRefGoogle Scholar
Hutchins, B. & Weber, J.T. (1985). The pretectal complex of the monkey: A reinvestigation of the morphology and retinal terminations. Journal of Comparative Neurology 232, 425442.Google Scholar
Johnson, R.F., Morin, L.P. & Moore, R.Y. (1988). Retinohypothalamic projections in the hamster and rat demonstrated using cholera toxin. Brain Research 462, 301312.CrossRefGoogle ScholarPubMed
Jones, E.G. (1985). The Thalamus. New York: Plenum Press, pp. 1935.CrossRefGoogle Scholar
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319338.Google Scholar
Ledoux, J.E., Ruggiero, D.A. & Reis, D.J. (1985). Projections to the subcortical forebrain from anatomically defined regions of the medial geniculate body in the rat. Journal of Comparative Neurology 242, 182213.Google Scholar
Ledoux, J.E., Ruggiero, D.A., Forest, R., Stornetta, R. & Reis, D.J. (1987). Topographic organization of convergent projections to the thalamus from the inferior colliculus and spinal cord in the rat. Journal of Comparative Neurology 264, 123146.Google Scholar
Levine, J.D., Weiss, M.L., Rosenwasser, A.M. & Miselis, R.R. (1991). Retinohypothalamic tract in the female albino rat: A study using horseradish peroxidase conjugated to cholera toxin. Journal of Comparative Neurology 306, 344360.CrossRefGoogle Scholar
Majorossy, K., Rethelyi, M. & Szentagothai, J. (1995). The large glomerular synapse of the pulvinar. Journal für Himforschung 7, 415432.Google Scholar
Mason, C.A. & Robson, J.A. (1979). Morphology of retino-geniculate axons in the cat. Neuroscience 4, 7997.CrossRefGoogle ScholarPubMed
Mathers, L.H. (1972). The synaptic organization of cortical projection to pulvinar in squirrel monkey. Journal of Comparative Neurology 146, 4360.Google Scholar
McLean, I.W. & Nakane, P.K. (1974). Periodate-lysine-paraformaldehyde fixative: A new fixative for immunoelectron microscopy. Journal of Histochemistry and Cytochemistry 22, 10771083.Google Scholar
Meyer-Bernstein, E.L. & Morin, L.P. (1996). Differential serotonergic innervation of the suprachiasmatic nucleus and the intergeniculate leaflet and its role in circadian rhythm modulation. Journal of Neuroscience 16, 20972111.CrossRefGoogle ScholarPubMed
Miguel-Hidalgo, J.-J., Senba, E., Matsutani, S., Takatsuji, K., Fukui, H. & Tohyama, M. (1989). Laminar and segregated distribution of immunoreactivities for some neuropeptides and adenosine deaminase in the superior colliculus of the rat. Journal of Comparative Neurology 280, 410423.Google Scholar
Miguel-Hidalgo, J.-J., Senba, E., Takatsuji, K. & Tohyama, M. (1990). Substance P and enkephalins in the superficial layers of the rat superior colliculus: Differential plastic effects of retinal deafferentation. Journal of Comparative Neurology 299, 389404.CrossRefGoogle ScholarPubMed
Mikkelsen, J.D. (1992). Visualization of efferent retinal projections by immunohistochcmical identification of cholera toxin subunit B. Brain Research Bulletin 28, 619623.Google Scholar
Moore, R.Y. & Lenn, N.J. (1972). A retinohypothalamic projection in the rat. Journal of Comparative Neurology 146, 114.CrossRefGoogle ScholarPubMed
Morin, L.P., Blanchard, J.H. & Moore, R.Y. (1992). Intergeniculate leaflet and suprachiasmatic nucleus organization and connections in the hamster. Visual Neuroscience 8, 219230.Google Scholar
Morin, L.P. (1994). The circadian visual system. Brain Research Reviews 67, 102127.CrossRefGoogle Scholar
Morin, L.P. & Blanchard, J. (1995). Organization of the hamster intergeniculate leaflet: NPY and ENK projections to the suprachiasmatic nucleus, intergeniculate leaflet and posterior limitans nucleus. Visual Neuroscience 12, 5767.CrossRefGoogle Scholar
Nilsson, O.G., Brundin, P. & Björklund, A. (1990). Amelioration of spatial memory impairment by intrahippocampal grafts of mixed septal and raphe tissue in rats with combined cholinergic and serotonergic denervation of the forebrain. Brain Research 515, 193206.CrossRefGoogle ScholarPubMed
Paxinos, G. & Watson, C. (1986). The Rat Brain in Stereotaxic Coordinales, 2nd edition. New York: Academic.Google Scholar
Perry, V.H. & Cowey, A. (1979). Changes in the retino-fugal pathways following cortical and tectal lesions in neonatal and adult rats. Experimental Brain Research 35, 97108.Google Scholar
Pickard, G.E. & Silverman, A.J. (1981). Direct retinal projections to hypothalamus piriform cortex and accessory optic nuclei in the golden hamster as demonstrated by a sensitive anterograde horseradish peroxidase technique. Journal of Comparative Neurology 196, 155172.Google Scholar
Price, J.L. (1995). Thalamus. In The Rat Nervous System, ed. Paxinos, G., pp. 629648. New York: Academic.Google Scholar
Reese, D.E. (1988). ‘Hidden lamination’ in the dorsal lateral geniculate nucleus: The functional organization of this thalamic region in the rat. Brain Research Reviews 13, 119137.Google Scholar
Ritter, S. & Dinh, T.T. (1991). Prior optic nerve transection reduces capsaicin-induced degeneration in rat subcortical visual structures. Journal of Comparative Neurology 308, 7990.CrossRefGoogle ScholarPubMed
Robson, J.A. & Hall, W.C. (1977). The organization of the pul vinar in the grey squirrel (Sciurus carolinensis). II. Synaptic organization and comparisons with the dorsal lateral geniculate nucleus. Journal of Comparative Neurology 173, 389416.Google Scholar
Robson, J.A. & Mason, C.A. (1979). The synaptic organization of terminals traced from individual labeled retino-geniculate axons in the cat. Neuroscience 4, 99111.Google Scholar
Rose, J.E. (1942). The thalamus of the sheep: Cellular and fibrous structure and comparison with pig, rabbit, and cat. Journal of Comparative Neurology 77, 469523.CrossRefGoogle Scholar
Scalia, F. (1972). The termination of retinal axons in the pretectal region of mammals. Journal of Comparative Neurology 145, 223258.Google Scholar
Scalia, F. & Arango, V. (1979). Topographic organization of the projections of the retina to the pretectal region in the rat. Journal of Comparative Neurology 186, 271292.CrossRefGoogle Scholar
Schneider, J.E. (1970). Mechanisms of functional recovery following lesions of visual cortex or superior colliculus in neonate and adult hamsters. Brain, Behavior, and Evolution 3, 295323.Google Scholar
Sefton, A.J. & Dreher, B. (1995). Visual system. In The Rat Nervous System, ed. Paxinos, G., pp. 833898. New York: Academic.Google Scholar
Siminoff, R., Schwassmann, H.O. & Kruger, L. (1967). Unit analysis of the pretectal nuclear group in the rat. Journal of Comparative Neurology 130, 329342.Google Scholar
Simpson, J.I., Giolli, R.A. & Blanks, R.H.I. (1988). The pretectal nuclear complex and the accessory optic system. Reviews of Oculomotor Research 2, 335364.Google ScholarPubMed
Speh, J.C. & Moore, R.Y. (1993). Retinohypothalamic tract development in the hamster and rat. Developmental Brain Research 76, 171181.Google Scholar
Swanson, Lav. (1992). Brain Maps: Structure of the Rat Brain. New York: Elsevier, pp. 1240.Google Scholar
Szentagothai, J., Hamori, J. & Tombol, T. (1966). Degeneration and electron microscope analysis of the synaptic glomeruli in the lateral geniculate body. Experimental Brain Research 2, 283301.Google Scholar
Takatsuji, K. & Tohyama, M. (1993). Differential effects on substance P immunoreactivity in the rat suprachiasmatic and olivary pretectal nuclei. Neuroreport 4, 647650.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, 131142.CrossRefGoogle ScholarPubMed
Tiao, Y.-C. & Blakemore, C. (1976). Functional organization in the visual cortex of the golden hamster. Journal of Comparative Neurology 168, 459482.Google Scholar
Weber, J.T. & Harting, J.K. (1980). The efferent projections of the pretectal complex: An autoradiographic and horseradish peroxidase analysis. Brain Research 194, 128.CrossRefGoogle ScholarPubMed
Weber, J.T. & Hutchins, B. (1982). The demonstration of a retinal projection to the medial pretectal nucleus in the domestic cat and the squirrel monkey: An autoradiographic analysis. Brain Research 232, 181186.Google Scholar
Winer, J.A., Morest, O.K. & Diamond, I.T. (1988). A cytoarchitectonic atlas of the medial geniculate body of the opossum, Didelphys viginiana, with a comment on the posterior intralaminar nuclei of the thalamus. Journal of Comparative Neurology 274, 422448.CrossRefGoogle Scholar
Yamazoe, M., Shiosaka, S., Emson, P.C. & Tohyama, M. (1985). Distribution of neuropeptide Y in the lower brainstem: An immunohisto-chemical analysis. Brain Research 335, 109120.Google Scholar
Youngstrom, T.G., Weiss, M.L. & Nunez, A.A. (1987). A retinal projection to the paraventricular nuclei of the hypothalamus in the Syrian hamster (Mesocricetus auratus). Brain Research Bulletin 19, 747750.Google Scholar
Youngstrom, T.G., Weiss, M.L. & Nunez, A.A. (1991). Retinofugal projections to the hypothalamus, anterior thalamus and basal forebrain in hamsters. Brain Research Bulletin 26, 403411.Google Scholar
Zhang, H.Y. & Hoffmann, K.-P. (1993). Retinal projections to the pretectum, accessory optic system and superior colliculus in pigmented and albino ferrets. European Journal of Neuroscience 5, 486500.CrossRefGoogle Scholar