Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-23T05:06:09.849Z Has data issue: false hasContentIssue false
  • English
  • Français

Postnatal development of substance-P immunoreactivity in the rat superior colliculus

Published online by Cambridge University Press:  02 June 2009

M. Behan ,
P. P. Appell  and
N. Kime
M. Behan
Affiliation:
Department of Comparative Biosciences, School of Veterinary Medicine, University of Wisconsin, Madison
P. P. Appell
Affiliation:
Department of Comparative Biosciences, School of Veterinary Medicine, University of Wisconsin, Madison
N. Kime
Affiliation:
Department of Comparative Biosciences, School of Veterinary Medicine, University of Wisconsin, Madison
Get access Rights & Permissions [Opens in a new window]

Abstract

Immunocytochemical techniques have been used to examine the distribution of substance-P (SP)-labeled neurons in the superior colliculus of rats from birth to adulthood. At birth, there are almost no SP-immunopositive neurons in the tectum. A small number of SP neurons appear over the next several days. However, the vast majority of SP neurons appear between P9 and P10, and by P12 have attained adult-like numbers and distribution. Neurons are confined to the superficial layers of the colliculus, specifically the upper two-thirds of the stratum griseum superficiale (SGS). There is no indication of a differential developmental sequence along rostrocaudal or mediolateral axes. Neuronal types can be distinguished as early as P6 and include horizontal, vertical, and multipolar cells.

Substance-P-immunoreactive axons and boutons are also present in the superior colliculus at birth, and are for the most part confined to the deep layers. Boutons are generally of the en-passant type. The density of labeled axons and boutons increases progressively, and by P10 there is an almost adult-like lamination and patchiness. In the adult, labeled axons and boutons are most dense in the stratum opticum and stratum griseum intermedium. Bridges of dorsoventrally oriented labeled axons span the relatively label-poor stratum album intermedium. SP label in the stratum griseum profundum is dense and patchy, and there is also dense label in the stratum album profundum bordering the periaqueductal grey.

The role of substance-P-labeled neurons in the superior colliculus is still a matter of speculation. The findings of this study indicate that SP neurons may play a role in intrinsic collicular circuitry.

Keywords

MammalianTectumVisual
Type
Research Articles
Information
Visual Neuroscience , Volume 10 , Issue 6 , November 1993 , pp. 1121 - 1127
Copyright
Copyright © Cambridge University Press 1993

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

Albers, F.J. (1990). Structure and Organization of the Superior Col-liculus of the Rat. Amsterdam: Thesis Publishers.Google Scholar
Behan, M. & Appell, P.P. (1992). Intrinsic circuitry in the cat superior colliculus: Projections from the superficial layers. Journal of Comparative Neurology 315, 230–243.Google Scholar
Bennett-Clarke, C, Mooney, R.D., Chiaia, N.L. & Rhoades, R.W. (1989). A substance-P projection from the superior colliculus to the parabigeminal nucleus in the rat and hamster. Brain Research 500, 1–11.CrossRefGoogle Scholar
Brecha, N., Sharma, S.C. & Karten, H.J. (1981). Localization of sub-stance-P-like immunoreactivity in the adult and developing goldfish retina. Neuroscience 6, 2737–2746.CrossRefGoogle ScholarPubMed
Brecha, N., Hendrickson, A., Floren, I. & Karten, H.J. (1982). Localization of substance-P-like immunoreactivity within the monkey retina. Investigative Ophthalmology 23, 147–153.Google Scholar
Brecha, N., Johnson, D., Bolz, J., Sharma, S., Parnavelas, J.G. & Lieberman, A.R. (1987). Substance-P-immunoreactive retinal ganglion cells and their central axon terminals in the rabbit. Nature (London) 327, 155–158.CrossRefGoogle ScholarPubMed
Chigr, F., Najimi, M., Leduque, P., Chayvialle, J.A., Bouvier, R. & Kopp, N. (1991). Anatomical distribution of substance-P-immunoreactive neurons in human brain stem during the first postnatal year. Brain Research Bulletin 26, 515–523.Google Scholar
Cuello, A.C., Galfre, G. & Milstein, C. (1978). Detection of substance-P in the central nervous system by a monoclonal antibody. Proceedings of the National Academy of Sciences of the U.S.A. 76, 3532–3536.Google Scholar
DeCarlos, J.A. & O'leary, d.D.M. (1990). Subplate neurons “pioneer” the output pathway of the cortex but not pathways to brainstem or spinal targets. Society for Neuroscience Abstracts 16, 311.Google Scholar
del Rio, J.A., Soriano, E. & Ferrer, I. (1991). A transitory population of substance-P-like immunoreactive neurons in the developing cerebral cortex of the mouse. Developmental Brain Research 64, 205–211.Google Scholar
Erlich, D., Keyser, K.T. & Karten, H.J. (1987). Distribution of substance-P-like immunoreactive retinal ganglion cells and their pattern of termination in the optic tectum of chick (Gallus gallus). Journal of Comparative Neurology 266, 220–233.Google Scholar
Fosse, V.M., Heggelund, P. & Fonnum, F. (1989). Postnatal development of glutamatergic, GABAergic, and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats. Journal of Neuroscience 9, 426–435.CrossRefGoogle ScholarPubMed
Frost, D.O., So, K.-F. & Schneider, G.E. (1979). Postnatal development of retinal projections in Syrian hamster: A study using auto-radiographic and anterograde degeneration techniques. Neuroscience 4, 1649–1677.CrossRefGoogle Scholar
Huerta, M.F. & Harting, J.K. (1984). The mammalian superior colliculus: Studies of its morphology and connections. In Comparative Neurology of the Optic Tectum, ed. Vanegas, H., pp. 687–773. New York: Plenum Press.Google Scholar
Huntley, G.W., Hendry, S.H.C., Killackey, H.P., Chalupa, L.M. & Jones, E.G. (1988). Temporal sequence of neurotransmitter expression by developing neurons in fetal monkey visual cortex. Developmental Brain Research 43, 69–96.CrossRefGoogle Scholar
Hutsler, J.J. & Chalupa, L.M. (1991). Substance-P immunoreactivity identifies a projection from the cat's superior colliculus to the principal tectorecipient zone of the lateral posterior nucleus. Journal of Comparative Neurology 312, 379–390.CrossRefGoogle Scholar
Ishimoto, I., Shiosaka, S., Skimizu, Y., Kuwayama, Y., Fukuda, M., Inagaki, S., Tagaki, H., Sakanaka, M., Takatsuki, K., Senba, E. & Tohyama, M. (1982). Two types of substance-P-containing cells and their uneven distribution in the chicken retina: An immunohistochemical analysis within flatmounts. Brain Research 240, 171–174.CrossRefGoogle ScholarPubMed
Kobayashi, N., Sakuma, M., Yoshioka, K., Onishi, Y., Yanagisawa, M., Kawashima, K. & Otsuka, M. (1991). Substance-P-evoked release of acetylcholine from isolated spinal cord of the newborn rat. Neuroscience 45, 331–337.CrossRefGoogle ScholarPubMed
Land, P.W. & Lund, R.D. (1979). Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science 205, 698–700.CrossRefGoogle ScholarPubMed
Ljungdahl, A., Hokfelt, T. & Nilsson, G. (1978). Distribution of sub-stance-P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals. Neuroscience 3, 861–943.CrossRefGoogle Scholar
Lord, Plummer K. & Behan, M. (1993). Development of corticotectal synaptic terminals in the cat: A quantitative electron microscopic analysis. Journal of Comparative Neurology (in press).Google Scholar
Lund, R.D. & Lund, J.S. (1972). Development of synaptic patterns in the superior colliculus of the rat. Brain Research 42, 1–20.Google Scholar
Lund, R.D. & Bunt, A.H. (1976). Prenatal development of central optic pathways in albino rats. Journal of Comparative Neurology 165, 247–264.CrossRefGoogle ScholarPubMed
McHaffie, J.G., Ogasawara, K. & Stein, B.E. (1983). Ascending non-visual afferents to the superior colliculus in neonatal kittens. Society for Neuroscience Abstracts 9, 379.Google Scholar
McHaffie, J.G., Beninato, M., Stein, B.E. & Spencer, R.F. (1991). Postnatal development of acetylcholinesterase in, and cholinergic projections to, the cat superior colliculus. Journal of Comparative Neurology 313, 113–131.Google Scholar
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 adeno-sine deaminase in the superior colliculus of the rat. Journal of Comparative Neurology 280, 410–423.CrossRefGoogle Scholar
Miguel-Hidalgo, J.J., Senba, E., Takatsuji, K. & Tohyama, M. (1991). Effects of eye enucleation on substance-P-immunoreactive fibers of some retinorecipient nuclei of the rat in relation to their origin from the superior colliculus. Neuroscience 44, 235–243.Google Scholar
Mize, R., Spencer, R.F. & Sterling, P. (1982). Two types of GABA-accumulating neurons in the superficial layers of the cat superior colliculus. Journal of Comparative Neurology 206, 180–192.Google Scholar
Mooney, R.D., Nikoletseas, M.M., Ruiz, S.A. & Rhoades, R.W. (1988). Receptive-field properties and morphological characteristics of the superior collicular neurons that project to the lateral posterior and dorsal lateral geniculate nuclei of the hamster. Journal of Neurophysiology 59, 1333–1351.CrossRefGoogle Scholar
Nakagawa, S., Hasegawa, Y., Kubozono, T. & Takumi, K. (1988). Substance-P-like immunoreactive retinal terminals found in two retinorecipient areas of the Japanese monkey. Neuroscience Letters 93, 32–37.Google Scholar
Ni, L. & Jonakait, G.M. (1988). Development of substance-P-containing neurons in the central nervous system in mice: An immunocytochemical study. Journal of Comparative Neurology 275, 493–510.Google Scholar
Ogawa-Meguro, R., Itoh, K. & Mizuno, N. (1992). Substance-P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateal geniculate nucleus in the rat. Experimental Brain Research 89, 59–66.Google Scholar
Osborne, N.N., Nicholas, D.A., Dockray, G.J. & Cuello, A.C. (1982). Cholecystokinin and substance-P immunoreactivity in retinas of rats, frogs, lizards, and chicks. Experimental Eye Research 34, 639–649.Google Scholar
Pickel, V.M., Sumal, K.K. & Miller, R.J. (1982). Early prenatal development of substance-P- and enkephalin-containing neurons in the rat. Journal of Comparative Neurology 210, 411–422.CrossRefGoogle ScholarPubMed
Ramirez, J.J., Jhaveri, S., Hahm, J.O. & Schneider, G.E. (1990). Maturation of projections from occipital cortex to the ventrolateral geniculate and superior colliculus in postnatal hamsters. Developmental Brain Research 55, 1–9.Google Scholar
Rhoades, R.W., Rohrer, W.H., Mooney, R.D. & Ruiz, S. (1989 a). The orientation of horizontal cell dendrite in the superior colliculus of the hamster: An analysis based on three-dimensional reconstruction of intracellularly injected neurons. Experimental Brain Research 76, 229–238.CrossRefGoogle ScholarPubMed
Rhoades, R.W., Mooney, R.D., Rohrer, W.H., Nikoletseas, M.M. & Fish, S.E. (1989 b). Organization of the projection from the superficial to the deep layers of the hamster's superior colliculus as demonstrated by the anterograde transport of Phaseolus vulgaris Leucoagglutinin. Journal of Comparative Neurology 283, 54–70.CrossRefGoogle Scholar
Rhoades, R.W., Figley, B., Mooney, R.D. & Fish, S.E. (1991). Development of the occipital corticotectal projection in the hamster. Experimental Brain Research 86, 373–383.Google Scholar
Sakuma, M., Yoshioka, K., Suzuki, H., Yanagisawa, M., Onishi, Y., Kabayashi, N. & Otsuka, M. (1991). Substance-P-evoked release of GABA from isolated spinal cord of the newborn rat. Neuroscience 45, 323–330.Google Scholar
Schliebs, R. & Rothe, T. (1988). Development of GABAA receptors in the central visual structures of rat brain. Effect of visual pattern deprivation. General Physiology and Biophysics 7, 281–292.Google Scholar
Stein, B.E. (1984). Development of the superior colliculus. Annual Review of Neuroscience 7, 95–125.Google Scholar
Takatsuji, K., Miguel-Hidalgo, J.-J., Hagihira, S. & Tohyama, M. (1990). Appearance of substance-P-like immunoreactive neurons in the rat superior colliculus after neonatal enucleation. Developmental Brain Research 54, 11–19.Google Scholar
Thong, I.G. & Dreher, B. (1986). The development of the corticotectal pathway in the albino rat. Developmental Brain Research 25, 227–238.CrossRefGoogle Scholar
Wadhwa, S., Rath, S., Jotwani, G. & Bijlani, V. (1990). Development of substance-P, leuenkephalin, and serotonin profiles in the lateral geniculate nuclear complex of albino rat. Neuroscience Letters 120, 146–150.Google Scholar
Wahle, P. (1993). Differential regulation of substance-P and somato-statin in Marinotti cells of the developing visual cortex. Journal of Comparative Neurology 329, 519–538.Google Scholar
Warton, S.S. & McCart, R. (1989). Synaptogenesis in the stratum griseum superficiale of the rat superior colliculus. Synapse 3, 136–148.Google Scholar
Williams, R.W. & Chalupa, L.M. (1982). Prenatal development of retinocollicular projections in the cat: An anterograde tracer transport study. Journal of Neuroscience 2, 604–622.CrossRefGoogle Scholar
Wolf, S.S., Moody, T.W., Quirion, R. & O'Donoghue, T.L. (1985). Biochemical characterization and autoradiographic localization of central substance-P receptors using (125I) Physalaemin. Brain Research 332, 299–307.Google Scholar
Yamashita, A., Shimazu, K. & Hayashi, M. (1990). Ontogeny of substance-P-immunoreactive structures in the primate cerebral neocortex. Developmental Brain Research 57, 197–207.Google Scholar