Skip to main content
SpringerLink
Log in

Substance P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateral geniculate nucleus in the rat

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Substance P (SP)-, vasoactive intestinal polypeptide (VIP)-, and cholecystokinin (CCK)-like immunoreactive (LI) neurons were found in the superior colliculus (SC) of the rat, and examined to ascertain whether they sent projection fibers to the dorsal lateral geniculate nucleus (LGNd). Immunocytochemical staining with antisera against SP, VIP, and CCK showed that many immunoreactive neuronal cell bodies were located in the superficial layers of the SC, especially in the stratum griseum superficiale. The pattern of distribution of these immunoreactive neuronal cell bodies in the SC was similar to that of neuronal cell bodies which were retrogradely labeled with WGA-HRP (wheat germ agglutinin-horseradish peroxidase conjugate) injected ipsilaterally into the LGNd. On the other hand, SP-, VIP- and CCK-LI axons were seen most densely in the lateral part of the LGNd, especially in the small-celled LGNd zone adjacent to the optic tract, where anterograde labeling was also observed after injection of WGA-HRP ipsilaterally into the superficial layers of the SC. When a lesion was produced by kainic acid injection into the superficial layers of the SC, axons showing SP-, VIP-, or CCK-LI in the LGNd ipsilateral to the lesion were markedly depleted. The results indicate that SC-LGNd projection neurons contain SP, VIP, and/or CCK in the rat.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Albano JE, Norton TT, Hall WC (1979) Laminar origin of projections from the superficial layers of the superior colliculus in the tree shrew, Tupaia glis. Brain Res 173:1–11

    Google Scholar 

  • Balkema GW Jr, Pinto LH (1982) Electrophysiology of retinal ganglion cells in the mouse: a study of a normally pigmented mouse and a congenic hypopigmentation mutant, Pearl. J Neurophysiol 48:968–980

    Google Scholar 

  • Bennett-Clarke C, Mooney RD, Chiaia NL, Rhoades RW (1989) A substance P projection from the superior colliculus to the parabigeminal nucleus in the rat and hamster. Brain Res 500:1–11

    Google Scholar 

  • Berson DM (1987) Retinal W-cell input to the upper superficial gray layer of the cat's superior colliculus: a conduction-velocity analysis. J Neurophysiol 58:1035–1051

    Google Scholar 

  • Brauer K, Schober W, Winkelmann E, Garey LJ (1988) Topographie differences in retinal axons in the dorsal lateral geniculate nucleus of the rat: a quantitative reexamination using anterograde transport of horseradish peroxidase. Exp Brain Res 69:481–488

    Google Scholar 

  • Cleland BG, Levick WR, Morstyn R, Wagner HG (1976) Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. J Physiol (Lond) 255:299–320

    Google Scholar 

  • Dräger UC, Hubel DH (1975) Responses to visual stimulation and relationship between visual, auditory, and somotosensory inputs in mouse superior colliculus. J Neurophysiol 38:690–713

    Google Scholar 

  • Fukuda Y (1977) A three-group classification of rat retinal ganglion cells: histological and physiological studies. Brain Res 119:327–344

    Google Scholar 

  • Fukuda Y, Sumitomo I, Sugitani M, Iwama K (1980) Distribution of fast and slow principal cells in the rat dorsal lateral geniculate nucleus. In: Ito M, Tsukahara N, Kubota K, Yagi K (eds) Integrative control functions of the brain, Vol III. Kodansha, Tokyo/Elsevier, Amsterdam, pp. 72–74

    Google Scholar 

  • Fukuda Y, Suzuki DA, Iwama K (1978) Characteristics of optic nerve innervation in the rat superior colliculus as revealed by field potential analysis. Jpn J Physiol 28:347–365

    Google Scholar 

  • Gabriel S, Gabriel H-J, Zippel U, Brandi H (1985) Regional distribution of fast and slow geniculo-cortical relay cells (GCR-cells) within the rat's dorsal lateral geniculate nucleus (LGNd). Exp Brain Res 61:210–213

    Google Scholar 

  • Graham J, Berman N (1981) Origins of the projections of the superior colliculus to the dorsal lateral geniculate nucleus and the pulvinar in the rabbit. Neurosci Lett 26:101–106

    Google Scholar 

  • Graham J, Casagrande VA (1980) A light microscopic and electron microscopic study of the superficial layers of the superior colliculus of the tree shrew (Tupaia glis). J Comp Neurol 191:133–151

    Google Scholar 

  • Guillery RW (1970) The laminar distribution of retinal fibers in the dorsal lateral geniculate nucleus of the cat: a new interpretation. J Comp Neurol 138:339–368

    Google Scholar 

  • Hale PT, Sefton AJ, Dreher B (1979) A correlation of receptive field properties with conduction velocity of cells in the rat's retinogeniculo-cortical pathway. Exp Brain Res 35:425–442

    Google Scholar 

  • Harrel JV, Caldwell RB, Mize RR (1982) The superior colliculus neurons which project to the dorsal and ventral lateral geniculate nuclei in the cat. Exp Brain Res 46:234–242

    Google Scholar 

  • Harting JK, Casagrande VA, Weber JT (1978) The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradiographic demonstration of interlaminar distribution of tectogeniculate axons. Brain Res 150:593–599

    Google Scholar 

  • Harting JK, Huerta MF, Hashikawa T, van Lieshout DP (1991) Projection of the mammalian superior colliculus upon the dorsal lateral geniculate nucleus: organization of tectogeniculate pathways in nineteen species. J Comp Neurol 304:275–306

    Google Scholar 

  • Hatanaka H, Amano T (1981) A mouse neuroblastoma X rat glioma hybrid cell produces immunoreactive substance P-like material. Brain Res 215:305–316

    Google Scholar 

  • Hofbauer A, Dräger UC (1985) Depth segregation of retinal ganglion cells projecting to mouse superior colliculus. J Comp Neurol 234:4654–74

    Google Scholar 

  • Hsu SM, Raine L, Fanger H, (1981) Use of avidin-biotinperoxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29:577–580

    Google Scholar 

  • Huerta MF, Harting JK (1983) Sublamination within the superficial gray layer of the squirrel monkey: an analysis of the tectopulvinar projection using anterograde and retrograde transport methods. Brain Res 261:119–126

    Google Scholar 

  • Huerta MF, Harting JK (1984) Connectional organization of the superior colliculus. Trends Neurosci 7:286–289

    Google Scholar 

  • Itoh K, Conley M, Diamond IT (1981) Different distribution of large and small retinal ganglion cells in the cat after HRP injections of single layers of the lateral geniculate body and the superior colliculus. Brain Res 207:147–153

    Google Scholar 

  • Kawamura S, Fukushima N, Hattori S, Kudo M (1980) Laminar segregation of cells of origin of ascending projections from the superficial layers of the superior colliculus in the cat. Brain Res 184:486–490

    Google Scholar 

  • Kawamura S, Kobayashi E (1975) Identification of laminar origin of some tecto-thalamic fibers in the cat. Brain Res 91:281–285

    Google Scholar 

  • Larsson L-I (1981) A novel immunohistochemical model system for specificity and sensitivity screening of antisera against multiple antigens. J Histochem Cytochem 29:408–410

    Google Scholar 

  • Linden R, Perry VH (1983) Massive retinotectal projection in rats. Brain Res 272:145–149

    Google Scholar 

  • Ljungdahl A, Hökfelt T, Nilsson G (1978) Distribution of substance P-like immunoreactivity in the central nervous system of the rat. I. Cell bodies and nerve terminals. Neuroscience 3:861–943

    Article  CAS  PubMed  Google Scholar 

  • Lund RD, Cunningham TJ (1972) Aspects of synaptic and laminar organization of the mammalian lateral geniculate body. Invest Ophthalmol 11:291–302

    Google Scholar 

  • Lund RD, Lund JS, Wise RP (1974) The organization of the retinal projection to the dorsal lateral geniculate nucleus in pigmented and albino rats. J Comp Neurol 158:383–404

    Google Scholar 

  • MacKay-Sim A, Sefton AJ, Martin PR (1983) Subcortical projections to lateral geniculate and thalamic reticular nuclei in the hooded rat. J Comp Neurol 213:24–35

    Google Scholar 

  • McIlwain JT (1978) Cat superior colliculus: extracellular potentials related to W-cell synaptic actions. J Neurophysiol 41:1343–1358

    Google Scholar 

  • Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    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 adenosine deaminase in the superior colliculus of the rat. J Comp Neurol 280:410–423

    Google Scholar 

  • Montero VM, Brugge JF, Beitel RE (1968) Relation of the visual field to the lateral geniculate body of the albino rat. J Neurophysiol 31:221–236

    Google Scholar 

  • Mooney RD, Nikoletseas MM, Ruiz SA, Rhoades RW (1988) Receptive-field properties and morphological characteristics of the superior collicular neurons that project to the lateral posterior and dorsal lateral geniculate nuclei in the hamster. J Neurophysiol 59:1333–1351

    Google Scholar 

  • Ogawa R, Itoh K, Kaneko T, Mizuno N (1989) Co-existence of vasoactive intestinal polypeptide (VIP)- and cholecystokinin (CCK)-like immunoreactivities in thalamocortical neuron in the ventrolateral nucleus of the rat. Brain Res 490:152–156

    Google Scholar 

  • Ogawa T, Takahashi Y (1981) Retinotectal connectivities within the superficial layers of the cat's superior colliculus. Brain Res 217:1–11

    Google Scholar 

  • Pasquier DA, Villar MJ (1982) Subcortical projections to the lateral geniculate body in the rat. Exp Brain Res 48:409–419

    Google Scholar 

  • Perry VH (1979) The ganglion cell layer of the retina of the rat: a Golgi study. Proc R Soc (B) 204:363–375

    Google Scholar 

  • Perry VH (1980) A tectocortical visual pathway in the rat. Neuroscience 5:915–927

    Google Scholar 

  • Perry VH (1981) Evidence for an amacrine cell system in the ganglion cell layer of the rat retina. Neuroscience 6:931–944

    Google Scholar 

  • Reese BE (1984) The projection from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Brain Res 305:162–168

    Google Scholar 

  • Reese BE, Jeffery G (1983) Crossed and uncrossed visual topography in dorsal lateral geniculate nucleus of the pigmented rat. J Neurophysiol 49:877–885

    Google Scholar 

  • Rhoades RW, Chalupa LM (1979) Conduction velocity distribution of the retinal input to the hamster's superior colliculus and a correlation with receptive field characteristics. J Comp Neurol 184:243–264

    Google Scholar 

  • Robson JA, Hall WC (1976) Projections from the superior colliculus to the dorsal lateral geniculate nucleus of the grey squirrel (Sciureus carolinensis). Brain Res 113:379–385

    Google Scholar 

  • Rodieck RW (1979) Visual pathways. Ann Rev Neurosci 2:193–225

    Google Scholar 

  • Sachs GM, Schneider GE (1984) The morphology of optic tract axons arborizing in the superior colliculus of the hamster. J Comp Neurol 230:155–167

    Google Scholar 

  • Schober W, Gruschka H (1977) Die Ganglienzellen der Retina der Albinoratte: Eine qualitative und quantitative Studie. Z Mikrosk Anat Forsch 91:397–414

    Google Scholar 

  • Schober W, Gruschka H (1978) Zur Projektion der einzelnen Ganglienzellklassen der Retina der Albinoratte. Eine Studie mit Meerrettich-Peroxidase. Z Mikrosk Anat Forsch 92:283–297

    Google Scholar 

  • Sefton AJ (1968) The innervation of the lateral geniculate nucleus and anterior colliculus in the rat. Vision Res 8:867–881

    Google Scholar 

  • Sugimoto T, Mizuno N (1987) Quinolinic and kainic acids can enhance calcitonin gene-related peptide-like immunoreactivity in striatal neurons with substance P-like immunoreactivity. Brain Res 418:392–397

    Google Scholar 

  • Sugita S, Otani K, Tokunaga A, Terasawa K (1983) Laminar origin of the tecto-thalamic projections in the albino rat. Neurosci Lett 43:143–147

    Google Scholar 

  • Sumitomo I, Ide K, Iwama K, Arikuni T (1969) Conduction velocity of optic nerve fibers innervating lateral geniculate body and superior colliculus in the rat. Exp Neurol 25:378–392

    Google Scholar 

  • Taylor AM, Jeffery G, Lieberman AR (1986) Subcortical afferent and efferent connections of the superior colliculus in the rat and comparisons between albino and pigmented strains. Exp Brain Res 62:131–142

    Google Scholar 

  • Tiao Y-C, Blakemore C (1976) Regional specialization in the golden hamster's retina. J Comp Neurol 168:439–458

    Google Scholar 

  • Torrealba F, Partlow GD, Guillery RW (1981) Organization of the projection from the superior colliculus to the dorsal lateral geniculate nucleus of the cat. Neuroscience 6:1341–1360

    Google Scholar 

  • Vaney DI, Peichl L, Wässle H, Illing R-B (1981) Almost all ganglion cells in the rabbit retina project to the superior colliculus. Brain Res 212:447–453

    Google Scholar 

  • Wilson PD, Stone J (1975) Evidence of W-cell input in the cat's visual cortex via the C laminae of the lateral geniculate nucleus. Brain Res 92:472–478

    Google Scholar 

Download references

Author information

Author notes

  1. K. Itoh

    Present address: Department of Anatomy, 2nd Division, Gifu University School of Medicine, 500, Gifu, Japan

Authors and Affiliations

  1. Department of Morphological Brain Science, Faculty of Medicine, Kyoto University, 606, Kyoto, Japan

    R. Ogawa-Meguro, K. Itoh & N. Mizuno

Authors
  1. R. Ogawa-Meguro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. K. Itoh
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N. Mizuno
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ogawa-Meguro, R., Itoh, K. & Mizuno, N. Substance P-, vasoactive intestinal polypeptide-, and cholecystokinin-like immunoreactive fiber projections from the superior colliculus to the dorsal lateral geniculate nucleus in the rat. Exp Brain Res 89, 59–66 (1992). https://doi.org/10.1007/BF00229001

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00229001

Key words

Search

Navigation