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Intrinsic circuitry in the deep layers of the cat superior colliculus

Published online by Cambridge University Press:  02 June 2009

M. Behan
Affiliation:
Department of Comparative Biosciences, University of Wisconsin, Madison Cemer for Neuroscience, University of Wisconsin, Madison
N.M. Kime
Affiliation:
Department of Comparative Biosciences, University of Wisconsin, Madison

Abstract

The mammalian superior colliculus is involved in the transformation of sensory signals into orienting behaviors. Sensory and motor signals are integrated in the colliculus to produce movements of the eyes, head, and neck. While there is a considerable amount of information available on the afferent and efferent connections of the colliculus, almost nothing is known about its intrinsic circuitry, particularly that of its deepest layers. It is likely that intrinsic connections in these deeper layers of the colliculus participate in the sensory-motor transformations leading to orienting movements. In this study, we used the neuroanatomical tracer biocytin to label small groups of neurons in the deeper layers of the cat superior colliculus and examine the distribution of their axons and terminals. We found a broadly distributed network of intrinsic projections throughout the deep layers of the superior colliculus. While the majority of terminals were found in a 1–2 mm radius around the injection site, labeled terminals were found throughout the deep layers of the colliculus up to 5 mm from the injection site. In addition, these injections sometimes labeled terminals in the superficial tectum. Extensive projections were demonstrated by the more superficial injections, but few terminals were found when injections were confined to the deepest layers of the colliculus. There was no evidence of anisotropy in the distribution of terminals from injections made at different rostrocaudal or mediolateral locations; neurons located in any one region in the colliculus could potentially influence any other region. This network of intrinsic connections in the cat superior colliculus could provide a means for deeper-layer efferent neurons to associate, and to modulate or coordinate their output. Interneurons could also provide a substrate for mutual inhibition between neurons at the rostral pole of the colliculus that are active during fixation, and more caudally located neurons whose activity is associated with saccadic eye movements.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1996

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References

Aizawa, H., Gerfen, C.R. & Wurtz, R.H. (1995). Afferent connection to fixation zone of monkey superior colliculus from frontal cortex and basal ganglia. Society for Neurosciences A bstracts 21, 1194.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, 230243.CrossRefGoogle ScholarPubMed
Behan, M. & Kime, N.M. (1996). Spatial distributions of tectotectal connections in the cat. In Extrageniculostriate Mechanisms Underlying Visually-Guided Eye Movements, Progress in Brain Research, Vol. 112, ed. Norita, M., Bando, T. & Stein, B., pp. 131142, Holland, Eisevier, (in press).Google Scholar
Beitz, A.J., Clements, J.R., Mullett, M.A. & Ecklund, L.J. (1986). Differential origin of brainstem scrotoninergic projections to the midbrain periaqueductal gray and superior colliculus of the rat. Journal of Comparative Neurology 250, 498509.CrossRefGoogle Scholar
Chevalier, G., Deniau, J.M. & Menetrey, A. (1992). Evidence that biocytin is taken up by axons. Neuroscience Letters 140, 197199.CrossRefGoogle ScholarPubMed
Edwards, S.B. (1977). The commissural projection of the superior colliculus in the cat. Journal of Comparative Neurology 173, 2340.CrossRefGoogle ScholarPubMed
Edwards, S.B. (1980). The deep cell layers of the superior colliculus: Their reticular characteristics and structural organization. In The Reticular Formation Revisited, ed. Hobson, J.A. & Brazer, M.A.B., pp. 193209. New York: Raven Press.Google 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. 687773. New York: Plenum.CrossRefGoogle Scholar
Izzo, P.N. (1991). A note on the use of biocytin in anterograde tracing studies in the central nervous system: Application at both light and electron microscopic level. Journal of Neuroscience Methods 36, 155166.CrossRefGoogle ScholarPubMed
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319338.CrossRefGoogle ScholarPubMed
Keller, E.L. & Edelman, J.A. (1994). Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccadic burst cells in superior colliculus in monkey. Journal of Neurophysiology 12, 27542770.CrossRefGoogle Scholar
King, M.A., Louis, P.M., Hunter, B.E. & Walker, D.W. (1989). Biocytin: A versatile anterograde neuroanatomical tract-tracing alternative. Brain Research 497, 361367.CrossRefGoogle ScholarPubMed
Lee, C.L., Rohrer, W.H. & Sparks, D.L. (1988). Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332, 357360.CrossRefGoogle ScholarPubMed
Lee, P., Mirabal, R. & Hall, W.C. (1995). Intracollicular connections of the optic layer in the tree shrew. Society for Neuroscience Abstracts 21, 1193.Google Scholar
Magalhaes-Castro, H.H., Dorbela Da Lima, A., Saraiva, P.E.S. & Magalhaes-Castro, B. (1978). Horseradish peroxidase labeling of cat tecto-tectal cells. Brain Research 148, 113.CrossRefGoogle Scholar
McIlwain, J.T. (1975). Visual receptive fields and their images in superior colliculus of the cat. Journal of Neurophysiology 38, 219230.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1982). Lateral spread of neural excitation during microstimulation in intermediate gray layer of cat's superior colliculus. Journal of Neurophysiology 47, 167178.CrossRefGoogle ScholarPubMed
McIlwain, J.T. (1991). Distributed spatial coding in the superior colliculus: A review. Visual Neuroscience 6, 313.CrossRefGoogle ScholarPubMed
Meredith, M.A., Wallace, M.T. & Stein, B.E. (1992). Visual, auditory and somatosensory convergence in output neurons of the cat superior colliculus: Multisensory properties of the tecto-reticulo-spinal projection. Experimental Brain Research 88, 181186.CrossRefGoogle ScholarPubMed
Middlebrooks, J.C. & Knudsen, E.I. (1984). A neural code for auditory space in the cat's superior colliculus. Journal of Neuroscience 4, 26212635.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 adeno-sine deaminase in the superior colliculus of the rat. Journal of Comparative Neurology 280, 410423.CrossRefGoogle Scholar
Mize, R.R. (1992). The organization of GABAergic neurons in the mammalian superior colliculus. In GABA in the Retina and Central Visual System. Progress in Brain Research, Vol. 90, ed. Mize, R.R., Marc, R.E. & Sillito, A.M. pp. 219248. Holland: Elsevier.CrossRefGoogle Scholar
Mooney, R.D., Bennett-Clarke, C.A., King, T.D. & Rhoades, R.W. (1990). Tectospinal neurons in hamster contain glutamate-like immunoreactivity. Brain Research 537, 375380.CrossRefGoogle ScholarPubMed
Moschovakis, A.K. & Karabelas, A.B. (1985). Observations on the somatodendritic morphology and axonal trajectory of intracellularly HRP-labeled efferent neurons located in the deeper layers of the superior colliculus of the cat. Journal of Comparative Neurology 239, 276308.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1989). Fixation and orientation control by the tecto-reticulo-spinal-system in the cat whose head is unrestrained. Revue Neurologie (Paris) 145, 567579.Google ScholarPubMed
Munoz, D.P. & Guitton, D. (1991). Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. II. Sustained discharges during motor preparation and fixation. Journal of Neurophysiology 66, 16241641.CrossRefGoogle Scholar
Munoz, D.P. & Wurtz, R.H. (1993 a). Fixation zone of monkey superior colliculus. 1. Characteristics of fixation cells. Journal of Neurophysiology 70, 559575.CrossRefGoogle Scholar
Munoz, D.P. & Wurtz, R.H. (1993 b). Fixation zone of monkey superior colliculus. II. Reversible activation and deactivation. Journal of Neurophysiology 70, 576589.CrossRefGoogle Scholar
Munoz, D.P., Pelisson, D. & Guitton, D. (1991). Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251, 13581360.CrossRefGoogle ScholarPubMed
Otterson, O.P. & Storm-Mathisen, J. (1984). Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. Journal of Comparative Neurology 229, 374392.CrossRefGoogle Scholar
Peck, C.K. (1987). Saccade-related burst neurons in cat superior colliculus. Brain Research 408, 329333.CrossRefGoogle ScholarPubMed
Peck, C.K. (1990). Neuronal activity related to head and eye movements in cat superior colliculus. Journal of Physiology 421, 79104.CrossRefGoogle ScholarPubMed
Pourcho, R.G., Goebel, D.J., Jojich, L. & Hazlett, J.C. (1992). Immunocytochemical evidence for the involvement of glycine in sensory centers of the rat brain. Neuroscience 46, 643656.CrossRefGoogle ScholarPubMed
Smith, Y. (1992). Anterograde tracing with PHA-L and biocytin at the electron microscopic level. In Experimental Neuroanatomy: A Practical Approach, ed. Bolam, J.P. pp. 661679. New York: Oxford Press.Google Scholar
Spangler, K.M. & Morley, B.J. (1987). Somatostatin-like immunoreactivity in the midbrain of the cat. Journal of Comparative Neurology 260, 8797.CrossRefGoogle ScholarPubMed
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: Role of primate superior colliculus. Physiological Review 66, 118171.CrossRefGoogle ScholarPubMed
Sparks, D.L., Holland, R. & Guthrie, B.L. (1976). Size and distribution of movement fields in the monkey superior colliculus. Brain Research 113, 234.CrossRefGoogle ScholarPubMed
Stein, B.E. & Meredith, M.A. (1993). The Merging of the Senses. Cambridge: MIT Press.Google Scholar
Van Gisbergen, J.A.M., Van Opstal, A.J. & Tax, A.A.M. (1987). Collicular ensemble coding of saccades based on vector summation. Neuroscience 21, 541555.CrossRefGoogle ScholarPubMed
Vincent, S.R., McIntosh, C.H.S., Buchanan, A.M.J. & Bowen, J.C. (1985). Central somatostatin systems revealed with monoclonal antibodies. Journal of Comparative Neurology 238, 169186.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Goldberg, M.E. (1972). Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. Journal of Neurophysiology 35, 575586.CrossRefGoogle Scholar
Wurtz, R.H. & Mohler, C.W. (1976). Organization of monkey superior colliculus: Enhanced visual responses of visual layer cells. Journal of Neurophysiology 39, 745762.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Albano, J.E. (1980). Visual-motor function of the primate superior colliculus. Annual Review of Neuroscience 3, 189226.CrossRefGoogle ScholarPubMed
Wurtz, R.H., Goldberg, M.E. & Robinson, D.L. (1980). Behavioral modulation of visual responses in the monkey: Stimulus selection for attention and movement. Progress in Psychobiology and Physiological Psychology 9, 4383.Google Scholar
Wurtz, R.H. & Munoz, O.P. (1995). Role of monkey superior colliculus in control of saccades and fixation. In The Cognitive Neurosciences, ed. Gazzaniga, M.S., pp. 533547. Boston, Massachusetts: MIT Press.Google Scholar