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Laminar distribution and patchiness of cytochrome oxidase in mouse superior colliculus
Sidney I. Wiener,
Sidney I. Wiener
Eye Research Institute of the Retina Foundation, 20 Staniford St., Boston, Massachusetts 02114
Search for more papers by this authorSidney I. Wiener,
Sidney I. Wiener
Eye Research Institute of the Retina Foundation, 20 Staniford St., Boston, Massachusetts 02114
Search for more papers by this authorAbstract
The cytochrome oxidase (CO), acetylcholinesterase (AChE), myelin, and Nissl stains were studied and compared to develop an anatomical system identifying the laminar architecture of the mouse superior colliculus. The CO and myelin stains are shown to define collicular laminae more distinctly than does the Nissl stain. The layer of large rostrocaudally coursing fiber bundles that has formerly been referred to in the rodent literature as stratum album intermediale (SAI; layer V) is renamed as a sublayer of the stratum griseum intermediale (SGI; layer IV) to conform with the nomenclature for the cat superior colliculus of Kaneseki and Sprague ('74, J. Comp. Neurol. 158:319–338).
Patches of CO activity in layer IV (SGI) are shown that contain intensely stained, large, multipolar cell bodies. The CO patches do not correspond to those previously reported for AChE. The CO, myelin, and AChE stains all Indicate the presence of a large lateral extension termed the flank of layer IV (SGI). In contrast to the classical lamination pattern of the superior colliculus, the flank has no overlying layer II (stratum griseum superficiale, SGS) or layer III (stratum opticum, SO).
Literature Cited
- Antonetty, C. M., and K. E. Webster (1975) The organization of the spinotectal projection. An experimental study in the rat. J. Comp. Neurol. 163: 449–466.
- Arimatsu, Y., A. Seto, and T. Amano (1981) An atlas of α-bungarotoxin binding sites and structures containing acetylcholinesterase in the mouse central nervous system. J. Comp. Neurol. 198: 603–631.
- Beckstead, R. M., V. B. Domesick, and W. J. H. Nauta (1979) Efferent connections of the substantia nigra and ventral tegmental area in the rat. Brain Res. 175: 191–217.
- Budi Santoso, A. W., and Th. Bar (1984) Local cytochrome oxidase activity in the cerebral cortex of the rat, histochemically differentiated with the DAB-method. A micro-densitometric and electron microscope study. Adv. Exp. Med. Bio. 167: 281–289.
- Carroll, E. W., and M. T. T. Wong-Riley (1984) Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey. J. Comp. Neurol. 222: 1–17.
- Coulter, J. D., R. M. Bowker, S. P. Wise, E. A. Murray, A. J. Castiglioni, and K. N. Westlund (1979) Cortical, tectal and medullary descending pathways to the cervical spinal cord. In R. Granit and O. Pompeiano (eds): Reflex Control of Posture and Movement, Progress in Brain Research. Amsterdam: Elsevier, Vol. 50, pp. 263–274.
- Creutzfeldt. O. D. (1975) Neurophysiological correlates of different functional states of the brain. In D. H. Ingvar and N. A. Lassen (eds): Brain Work, Alfred Benzon Symposium VIII. N.Y.: Academic Press, pp. 21–46.
- Drager, U. C., and D. H. Hubel (1975) Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J. Neurophysiol. 38: 690–713.
- Drager, U. C., and D. H. Hubel (1976) Topography of visual and somatosensory projections to mouse superior colliculus. J. Neurophysiol. 39: 91–101.
- Edwards, S. B. (1977) The commissural projection of the superior colliculus in the cat. J. Comp. Neurol. 173: 23–40.
- Edwards, S. B. (1980) The deep cell layers of the superior colliculus:Their reticular characteristics and structural organization. In J. A. Hobson and M. A. B. Brazier (eds): The Reticular Formation Revisited. N.Y.: Raven Press, pp. 193–209.
- Edwards, S. B., C. L. Ginsburgh, C. K. Henkel, and B. E. Stein (1979) Sources of subcortical projections to the superior colliculus in the cat. J. Comp. Neurol. 184: 309–330.
- Feldman, S. G., and L. Kruger (1980) An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J. Comp. Neurol. 192: 427–454.
-
Fish, S. E.,
D. K. Goodman,
D. C. Kuo,
J. D. Polcer, and
R. W. Rhoades
(1982)
The intercollicular pathway in the golden hamster: An anatomical study.
J. Comp. Neurol.
204:
6–20.
10.1002/cne.902040103 Google Scholar
- Gallyas, F. (1979) Silver stain of myelin by means of physical development. Neurol. Res. 1: 203–209.
- Geneser-Jensen, F. A., and T. W. Blackstadt (1971) Distribution of acetylcholinesterase in the hippocampal region of the guinea pig- I. Entorhinal area, parasubiculum and presubiculum. Z. Zellforsch. 114: 460–481.
- Goldberg, M. E., and D. L. Robinson (1978) Visual system:Superior colliculus. In B. Masterson (ed): Handbook of Behavioral Neurobiology. N.Y.: Plenum, pp. 119–165.
- Gordon, B. (1975) Superior colliculus: Structure, physiology and possible functions. Int. Rev. Physiol. 3: 185–230.
- Graybiel, A. M. (1978a) A stereometric pattern of distribution of acetylthiocholinesterase in the deep layers of the superior colliculus. Nature 272: 539–541.
- Graybiel, A. M. (1978b) Organization of the nigrotectal connection: An experimental tracer study in the cat. Brain Res. 143: 339–348.
-
Graybiel, A. M.
(1979)
Periodic compartmental distribution of acetylcholinesterase in the superior colliculus of the human brain.
Neuroscience
4:
643–650.
10.1016/0306-4522(79)90140-4 Google Scholar
- Graybiel, A. M., N. Brecha, and H. J. Karten (1984) Cluster-and-sheet pattern of enkephalin-like immunoreactivity in the superior colliculus of the cat. Neuroscience 12: 191–214.
- Hendrickson, A. E., S. P. Hunt, and J.-Y. Wu (1981) Immunocytochemical localization of glutamic acid decarboxylase in monkey striate cortex. Nature 292: 605–607.
- Hess, A. (1960) The effects of eye removal on the development of cholinesterase in the superior colliculus. J. Exp. Zool. 144: 11–23.
- Hess, D. T., and B. H. Marker (1983) Technical modifications of Gallyas' silver stain for myelin. J. Neurosci. Methods 8: 95–97.
- Hoover, D. B., E. A. Muth, and D. M. Jacobowitz (1978) A mapping of the distribution of acetylcholine, choline acetyltransferase and acetylcholinesterase in discrete areas of rat brain. Brain Res. 153: 295–306.
- Horton, J. C., and D. H. Hubel (1981) Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292: 762–764.
- Huerta, M. F., A. Frankfurter, and J. K. Harting (1981) The trigeminocollicular projection in the cat: Patch-like endings within the intermediate gray. Brain Res. 211: 1–13.
- Huerta, M. F., A. Frankfurter, and J. K. Harting (1983) Studies of the principal sensory and spinal trigeminal nuclei of the rat: Projections to the superior colliculus, inferior olive, and cerebellum. J. Comp. Neurol. 220: 147–167.
-
Huerta, M. F., and
J. K. Harting
(1982)
Projections of the superior colliculus to the supraspinal nucleus and cervical spinal cord gray of the cat.
Brain Res.
242:
326–331.
10.1016/0006-8993(82)90317-1 Google Scholar
- Huerta, M. F., and J. K. Harting (1984) The mammalian superior colliculus:Studies of its morphology and connections. In H. Vanegas (ed): Comparative Neurology of the Optic Tectum. N.Y.: Plenum, pp. 687–773.
- Illing, R.-B., and A. M. Graybiel (1985) Convergence of afferents from frontal cortex and substantia nigra onto acetylcholinesterase-rich patches of the cat's superior colliculus. Neuroscience 14: 455–482.
- Itaya, S. K., P. W. Itaya, and G. W. Van Hoesen (1984) Intracortical termination of the retino-geniculo-striate pathway studied with transsynaptic tracer (wheat germ agglutinin-horseradish peroxidase) and cytochrome oxidase staining in the macaque monkey. Brain Res. 304: 303–310.
- Kageyama, G. H., and M. T. T. Wong-Riley (1982) Histochemical localization of cytochrome oxidase in the hippocampus: Correlation with specific neuronal types and afferent pathways. Neuroscience 7: 2337–2361.
- Kanaseki, T., and J. M. Sprague (1974) Anatomical organization of pretectal nuclei and tectal laminae in the cat. J. Comp. Neurol. 158: 319–338.
- Killackey, H. P., and R. S. Erzurumlu (1981) Trigeminal projections to the superior colliculus of the rat. J. Comp. Neurol. 201: 221–242.
- Konig, J. F. R., and Klippel, R. A. (1963) The rat brain:A stereotaxic atlas of the forebrain and lower parts of the brain stem. Baltimore: Williams and Wilkins.
- Kuypers, H. G. J. M., and V. A. Maisky (1975) Retrograde axonal transport of horseradish peroxidase from spinal cord to brain stem cell groups in the cat. Neurosci. Lett. 1: 9–14.
- Murray, E. A., and J. D. Coulter (1982) Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Res. 243: 201–214.
- Nussbaumer, J.-C., and H. Van Der Loos (1985) An electrophysiological and anatomical study of projections to the mouse cortical barrelfield and its surroundings. J. Neurophysiol. 53: 686–698.
- Paxinos, G., and C. Watson (1982) The Rat Brain in Stereotaxic Coordinates. N.Y.: Academic Press.
- Peck, C. K. (1984) Saccade-related neurons in cat superior colliculus: Pandirectional movement cells with postsaccadic responses. J. Neurophysiol. 52: 1154–1168.
- Ramon-Moliner, E. (1972) Acetylthiocholinesterase distribution in the brain stem of the cat. Ergebn. Anat. Entwickl.-Gesch. 46: 1–53.
- Rhoades, R. W., and D. R. DellaCroce (1980) Cells of origin of the tectospinal tract in the golden hamster: An anatomical and electrophysiological investigation. Exp. Neurol. 67: 163–180.
- Rhoades, R. W., S. E. Fish, and T. J. Voneida (1981) Anatomical and electro-physiological demonstration of tectotectal pathway in the golden hamster. Neurosci. Lett. 21: 255–260.
-
Ribak, C. E.
(1981)
The histochemical localization of cytochrome oxidase in the dentate gyrus of the rat hippocampus.
Brain Res.
212:
169–174.
10.1016/0006-8993(81)90046-9 Google Scholar
-
Sandell, J. H.
(1984)
The distribution of hexokinase compared to cytochrome oxidase and acetylcholinesterase in the somatosensory cortex and the superior colliculus of the rat.
Brain Res.
290:
384–389.
10.1016/0006-8993(84)90962-4 Google Scholar
- Schiller, P. H. (1985) The superior colliculus and visual function. In I. Darian-Smith (ed): Handbook of Physiology-The Nervous System, Vol. 3. Bethesda: Am. Physiol. Soc., pp. 457–505.
- Sidman, R. L., J. B. Angevine, Jr., and E. T. Pierce (1971) Atlas of the mouse brain and spinal cord. Cambridge: Harvard U. Press.
- Siou, G. (1958) Distribution normale et variation experimentale de l'activite cholinesterasique au niveau des tubercules quadrijumeaux anterieurs chez Is Souris. C.R. Hebd. Seanc. Acad. Sci. (Paris) 246: 315–317.
- Sparks, D. L., and Pollack, J. G. (1977) The neural control of saccadic eye movements: The role of the superior colliculus. In B. A. Brooks and F. J. Bajandras (eds): Eye Movements,. N.Y.: Plenum, pp. 179–219.
- Stein, B., and Clamann, H. P. (1981) Control of pinna movements and sensorimotor register in cat superior colliculus. Brain Behav. Evol. 19: 180–92.
- Stein, B. E., B. Magalhaes-Castro, and L. Kruger (1976) Relationship between visual and tactile representations in cat superior colliculus. J. Neurophysiol. 39: 401–419.
- Szekely, G. (1973) Anatomy and synaptology of the optic tectum. In R. Jung (ed): Handbook of Sensory Physiology, Volume VII/3, Central Visual Information B. Berlin: Springer-Verlag, pp. 1–26.
-
Tashiro, T.,
M. Judo, and
S. Kawamura
(1980)
Discontinuous spatial distribution of the tectal afferents from the trigeminal nucleus in the cat.
Neurosci. Lett.
20:
249–252.
10.1016/0304-3940(80)90155-X Google Scholar
- Tokunaga, A., and K. Otani (1976) Dendritic patterns of neurons of rat superior colliculus. Exp. Neurol. 52: 189–205.
- Valverde, F. (1973) The neuropil in superficial layers of the superior colliculus of the mouse. Z. Anat. Entwickl.-Gesch. 142: 117–147.
- Viktorov, I. V. (1966) Neuronal structure of anterior corpora bigemina in insectivora and rodents. Arkh. Anat. Gistol. Embriol. 51: 82–89.
- Viktorov, I. V. (1968) Neuronal structure of corpora quadrigemina in the cat. Arkh. Anat. Gistol. Embriol. 54: 45–55.
- Welker, C. (1971) Microelectrode delineation of fine grain somatotopic organization of SmI cerebral neocortex in albino rat. Brain Res. 26: 259–275.
- Welker, C. (1976) Receptive fields of barrels in the somatosensory neocortex of the rat. J. Comp. Neurol. 166: 173–190.
- Wong-Riley, M. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrable with cytochrome oxidase histochemistry. Brain Res. 171: 11–28.
- Wong-Riley, M. T. T., and E. W. Carroll (1984a) Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in VII prestriate cortex of the squirrel monkey. J. Comp. Neurol. 222: 18–37.
- Wong-Riley, M., and E. W. Carroll (1984b) Effect of impulse blockage on cytochrome oxidase in monkey visual system. Nature 307: 262–264.
- Wong-Riley, M. T. T., S. M. Walsh, P. A. Leake-Jones, and M. M. Merzenich (1981) Maintenance of neuronal activity by electrical stimulation of unilaterally deafened cats demonstrable with cytochrome oxidase technique. Ann. Otol. Rhinol. Laryngol. 90 suppl 82: 30–32.
- Wong-Riley, M. T. T., and C. Welt (1980) Histochemical changes in cytochrome oxidase of cortical barrels after vibrissal removal in neonatal and adult mice. Proc. Natl. Acad. Sci. U.S.A. 77: 2333–2337.
- Wurtz, R. H., and J. E. Albano (1980) Visual-motor function of the primate superior colliculus. Ann. Rev. Neurosci. 3: 189–226.
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