Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-13T13:48:37.536Z Has data issue: false hasContentIssue false
  • English
  • Français

The laminar distribution of macaque tectobulbar and tectospinal neurons

Published online by Cambridge University Press:  02 June 2009

Paul J. May  and
John D. Porter
Paul J. May
Affiliation:
Departments of Anatomy and Ophthalmology, University of Mississippi Medical Center, Jackson
John D. Porter
Affiliation:
Department of Anatomy and Neurobiology and Department of Ophthalmology, University of Kentucky Medical Center, Lexington
Get access Rights & Permissions [Opens in a new window]

Abstract

The superior colliculus exerts its most direct influence over orienting movements, and saccades in particular, via its descending projections to the brain stem and spinal cord. However, while there is detailed physiological data concerning the generation of saccade-related activity in the primate superior colliculus, there is relatively little data on the detailed connectivity of this structure in primates. Consequently, retrograde transport techniques were utilized to determine the locations of the cells of origin of these descending pathways in macaque monkeys. Tectal cells that projected to the ipsilateral pontine reticular formation were mainly found in the deep gray layer and occasionally in the intermediate gray layer. Tectal cells that projected to the contralateral pontine reticular formation were predominantly located in the intermediate gray layer. The contralaterally projecting population could be subdivided into two groups. The cells in upper sublamina of the intermediate gray layer project primarily to the saccade-related regions of the paramedian reticular formation. Cells in the lower sublamina project primarily to more lateral regions of the pontine reticular formation and to the spinal cord. We conclude that the primate colliculus is provided with at least three descending output channels, which are likely to differ in their connections and functions. Specifically, it seems likely that the lower portion of the intermediate gray layer may be specialized to subserve combined head and eye orienting movements, while the upper sublamina subserves saccades.

Keywords

Superior colliculusTectumSaccadeGazeReticular formation
Type
Research Articles
Information
Visual Neuroscience , Volume 8 , Issue 3 , March 1992 , pp. 257 - 276
Copyright
Copyright © Cambridge University Press 1992

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

Anderson, M.E., Yoshida, M. & Wilson, V.J. (1971). Influence of superior colliculus on cat neck motoneurons. Journal of Neurophysiology 34, 898–907.CrossRefGoogle ScholarPubMed
Benevento, L.A. & Standage, G.P. (1983). The organization of projections of the retinorecipient and nonretinorecipient nuclei of the pretectal complex and layers of the superior colliculus to the lateral pulvinar and medial pulvinar in the macaque monkey. Journal of Comparative Neurology 217, 307–336.CrossRefGoogle Scholar
Berthoz, A. & Grantyn, A. (1986). Neuronal mechanisms underlying eye-head coordination. In Progress in Brain Research, Vol. 64, ed. Freund, H.-J., Buttner, U., Cohen, B. & Noth, J., pp. 325–343. Amsterdam: Elsevier Science.Google Scholar
Bickford, M.E. & Hall, W.C. (1989). Collateral projections of predorsal bundle cells of the superior colliculus in the rat. Journal of Comparative Neurology 283, 86–106.CrossRefGoogle ScholarPubMed
Castiglioni, A.J., Gallaway, M.C. & Coulter, J.D. (1978). Spinal projections from the midbrain in monkey. Journal of Comparative Neurology 178, 329–346.CrossRefGoogle ScholarPubMed
Dean, P., Redgrave, P., Sahibzada, N. & Tsunt, K. (1986). Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19, 367–380.CrossRefGoogle ScholarPubMed
Edwards, S.B. & Henkle, C.K. (1978). Superior colliculus connections with the extraocular motor nuclei. Journal of Comparative Neurology 179, 451–468.CrossRefGoogle ScholarPubMed
Edwards, S.B., Ginsburgh, C.L., Henkel, C.K. & Stem, B.E. (1979). Sources of subcortical projections to the superior colliculus in the cat. Journal of Comparative Neurology 184, 309–330.CrossRefGoogle Scholar
Ellard, C.G. & Goodale, M.A. (1986). The role of the predorsal bundle in head and body movements elicited by electrical stimulation of the superior colliculus of the Mongolian gerbil. Experimental Brain Research 64, 421–433.CrossRefGoogle ScholarPubMed
Fukushima, K. (1987). The interstitial nucleus of Cajal and its role in the control of movements of head and eyes. Progress in Neurobiology 29, 107–192.CrossRefGoogle ScholarPubMed
Funahashi, S., Bruce, C.J. & Goldman-Rakic, P.S. (1990). Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. Journal of Neurophysiology 63, 814–831.CrossRefGoogle ScholarPubMed
Gnadt, J.W. & Andersen, R.A. (1988). Memory related motor planning activity in posterior parietal cortex of macaque. Experimental Brain Research 70, 216–220.CrossRefGoogle ScholarPubMed
Grantyn, A. & Berthoz, A. (1985). Burst activity of identified tectoreticulo-spinal neurons in the alert cat. Experimental Brain Research 57, 417–421.CrossRefGoogle ScholarPubMed
Grantyn, A. & Grantyn, R. (1982). Axonal patterns and sites of termination of cat superior colliculus neurons projecting in the tectobulbo-spinal tract. Experimental Brain Research 46, 243–256.CrossRefGoogle ScholarPubMed
Graybiel, A.M. (1978). Organization of the nigrotectal connection: an experimental tracer study in the cat. Brain Research 143, 339–348.CrossRefGoogle ScholarPubMed
Hall, W.C. & May, P.J. (1984). The anatomical basis for sensorimotor transformations in the superior colliculus. In Contributions to Sensory Physiology, Vol. 8, ed. Neff, E.E., pp. 1–34. New York: Academic Press.Google Scholar
Harting, J.K. (1977). Descending pathways from the superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatto). Journal of Comparative Neurology 173, 583–612.CrossRefGoogle Scholar
Hartinc, J.K., Hall, W.C., Diamond, I.T. & Martin, G.F. (1973). Anterograde degeneration study of the superior colliculus in Tupia glis: evidence for a subdivision between superficial and deep layers. Journal of Comparative Neurology 148, 361–386.CrossRefGoogle Scholar
Hartino, J.K., Huerta, M.F., Hashikawa, T., Weber, J.T. & Van Lieshout, D.P. (1988). Neuroanatomical studies of the nigrotectal projection in the cat. Journal of Comparative Neurology 278, 615–631.CrossRefGoogle Scholar
Hashikawa, T. & Kawamura, K. (1977). Identification of cells of origin of tectopontine fibers in the cat superior colliculus: an experimental study with the horseradish peroxidase method. Brain Research 130, 65–79.CrossRefGoogle ScholarPubMed
Henkel, C.K. (1981). Afferent sources of a lateral midbrain tegmentum zone associated with the pinnae in the cat as mapped by retro-grade transport of horseradish peroxidase. Journal of Comparative Neurology 203, 213–226.CrossRefGoogle Scholar
Henkel, C.K. & Edwards, S.B. (1978). The superior colliculus control of pinna movements in the cat: possible anatomical connections. Journal of Comparative Neurology 182, 763–776.CrossRefGoogle ScholarPubMed
Hirai, T., Onodera, S. & Kawamura, K. (1982). Cerebellotectal projections studied in cats with horseradish peroxidase and tritiated amino acids axonal transport. Experimental Brain Research 48, 1–12.CrossRefGoogle ScholarPubMed
Holcombe, V. & Hall, W.C. (1981a). The laminar origin and distribution of the crossed tectoreticular pathways. Journal of Neuroscience 1, 1103–1112.CrossRefGoogle ScholarPubMed
Holcombe, V. & Hall, W.C. (1981b). Laminar origin of ipsilateral tectopontine pathways. Journal of Neuroscience 6, 255–260.CrossRefGoogle ScholarPubMed
Holstege, G. & Cowie, R.J. (1989). Projections from the rostral mesencephalic reticular formation to the spinal cord. Experimental Brain Research 75, 265–279.CrossRefGoogle ScholarPubMed
Huerta, M.F. & Harting, J.K. (1982a). Tectal control of spinal cord activity: neuroanatomical demonstration of pathways connecting the superior colliculus with the cervical spinal cord grey. Progress in Brain Research 57, 293–328.Google ScholarPubMed
Huerta, M.F. & Harting, J.K. (1982b). Projections of the superior colliculus to the supraspinal nucleus and the cervical spinal cord gray of the cat. Brain Research 242, 326–331.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.CrossRefGoogle Scholar
Huerta, M.F. & Kaas, J.H. (1990). Supplementary eye field as defined by intracortical microstimulation: connections in macaques. Journal of Comparative Neurology 293, 299–330.CrossRefGoogle ScholarPubMed
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1986). Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: I. Subcortical connections. Journal of Comparative Neurology 253, 415–439.CrossRefGoogle ScholarPubMed
Iwamoto, Y., Sasaki, S. & Suzuki, I. (1988). Descending cortical and tectal control of dorsal neck motoneurons via reticulospinal neurons in the cat. Progress in Brain Research 76, 97–108.CrossRefGoogle ScholarPubMed
Jayaraman, A., BattonR.R., III R.R., III & Carpenter, M.B. (1977). Nigrotectal projections in the monkey: an autoradiographic study. Brain Research 135, 147–152.CrossRefGoogle ScholarPubMed
Kanaseki, T. & Sprague, J.M. (1974). Anatomical organization of pretectal nuclei and tectal laminae in the cat. Journal of Comparative Neurology 158, 319–338.CrossRefGoogle ScholarPubMed
Kawamura, K. & Hashikawa, T. (1978). Cell bodies of origin of reticular projections from the superior colliculus in the cat: an experimental study with the use of horseradish peroxidase as a tracer. Journal of Comparative Neurology 182, 1–16.CrossRefGoogle Scholar
Keay, K., Westerby, G.W.M., Frankland, P., Dean, P. & Redgrave, P. (1990). Organization of the crossed tecto-reticulo-spinal projection in the rat – II. Electrophysiological evidence for separate output channels to the periabducens area and caudal medulla. Neuroscience 37, 585–601.CrossRefGoogle Scholar
Keller, E.L. (1979). Colliculoreticular organization in the oculomotor system. Progress in Brain Research 50, 725–734.CrossRefGoogle ScholarPubMed
Kunzle, H. & Akert, K. (1977). Efferent connections of cortical area 8 (frontal eye field) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. Journal of Comparative Neurology 173, 147–164.CrossRefGoogle ScholarPubMed
Langer, T.P. & Kaneko, C.R.S. (1990). Brainstem afferents to the oculomotor omnipause neurons in monkey. Journal of Comparative Neurology 295, 413–427.CrossRefGoogle Scholar
Langer, T.P., Kaneko, C.R.S., Scudder, C.A. & Fuchs, A.F. (1986). Afferents to the abducens nucleus in the monkey and the cat. Journal of Comparative Neurology 245, 379–400.CrossRefGoogle Scholar
Leichnetz, G.R. & Goldberg, M.E. (1988). Higher centers concerned with eye movement and visual attention: cerebral cortex and thalamus. In Neuroanatomy of the Oculomotor System, Reviews of Oculomotor Research, Vol. 2, ed. Buttner-Ennerver, J., pp. 365–429. Amsterdam: Elsevier Science.Google Scholar
Leichnetz, G.R., Spencer, R.F., Hardy, S.G.P. & Astruc, J. (1981). The prefrontal corticotectal projection in the monkey; an anterograde and retrograde horseradish peroxidase study. Neuroscience 6, 1023–1041.CrossRefGoogle ScholarPubMed
Lu, S.M., Lin, C.-S., Behan, M., Cant, N.B. & Hall, W.C. (1985). Glutamate decarboxylase immunoreactivity in the intermediate grey layer of the superior colliculus in the cat. Neuroscience 16, 123–131.CrossRefGoogle ScholarPubMed
Lynch, J.C., Graybiel, A.M. & Lobeck, L.J. (1985). The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. Journal of Comparative Neurology 235, 241–254.CrossRefGoogle ScholarPubMed
Ma, T.P., Cheng, H.W., Czech, J.A. & Rafols, J.A. (1990). Intermediate and deep layers of the macaque superior colliculus: a Golgi study. Journal of Comparative Neurology 295, 92–110.CrossRefGoogle ScholarPubMed
Ma, T.P., Graybiel, A.M. & Wurtz, R.A. (1991). Location of saccade-related neurons in the macaque colliculus. Experimental Brain Research 85, 21–35.CrossRefGoogle ScholarPubMed
Masino, T. & Grobstein, P. (1989). The organization of descending tectofugal pathways underlying orienting in the frog, Rana pipiens. Experimental Brain Research 75, 245–264.CrossRefGoogle ScholarPubMed
Matsuyama, T. & Kawamura, S. (1985). Cytoarchitectonic coincidence with the discontinuous connectional pattern in the deep layers of the superior colliculus in the rat. Neuroscience Research 2, 335–348.CrossRefGoogle ScholarPubMed
May, P.J. & Hall, W.C. (1983). Projections from motor structures to eye movement-related neurons in the superior colliculus. Anatomical Record 205, 127A.Google Scholar
May, P.J. & Hall, W.C. (1984). Relationships between the nigrotectal pathway and the cells of origin of the predorsal bundle. Journal of Comparative Neurology 226, 357–376.CrossRefGoogle ScholarPubMed
May, P.J. & Hall, W.C. (1986). The cerebellotectal pathway in the grey squirrel. Experimental Brain Research 65, 200–212.CrossRefGoogle ScholarPubMed
May, P.J., Hartwich-Young, R., Nelson, J., Sparks, D.L. & Porter, J.D. (1990a). Cerebellotectal pathways in the macaque: implications for collicular generation of saccades. Neuroscience 36, 305–324.CrossRefGoogle ScholarPubMed
May, P.J., Vidal, P.-P. & Baker, R. (1990b). Synaptic organization of tectal-facial pathways in cat. II. Synaptic potentials following mid-brain tegmentum stimulation. Journal of Neurophysiology 64, 381–402.CrossRefGoogle ScholarPubMed
McHaffie, J.G., Kao, C.Q. & Stein, B.E. (1989). Nociceptive neurons in rat superior colliculus: response properties, topography, and functional implications. Journal of Neurophysiology 62, 510–525.CrossRefGoogle ScholarPubMed
Mesulam, M. (1978). Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. Journal of Histochemistry and Cytochemistry 26, 106–117.CrossRefGoogle ScholarPubMed
Mohler, C.W. & Wurtz, R.H. (1976). Organization of monkey superior colliculus: Intermediate layer cells discharging before eye movements. Journal of Neurophysiology 39, 722–765.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988a). Structure-function relationships in the primate superior colliculus. I. Morphological classification of efferent neurons. Journal of Neurophysiology 60, 232–262.CrossRefGoogle ScholarPubMed
Moschovakis, A.K., Karabelas, A.B. & Highstein, S.M. (1988b). Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. Journal of Neurophysiology 60, 263–302.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. Reviews of Neurology (Paris) 145, 567–579.Google ScholarPubMed
Murray, E.A. & Coulter, J.D. (1982). Organization of tectospinal neurons in the cat and rat superior colliculus. Brain Research 243, 210–214.CrossRefGoogle Scholar
Nudo, R.J. & Masterton, R.B. (1988). Descending pathways to the spinal cord: I. A comparative study of 22 mammals. Journal of Comparative Neurology 277, 53–79.CrossRefGoogle Scholar
Nudo, R.J. & Masterton, R.B. (1989). Descending pathways to the spinal cord: II. Quantitative study of the tectospinal tract in 23 mammals. Journal of Comparative Neurology 286, 96–119.CrossRefGoogle Scholar
Peele, T.L. (1942). Cytoarchitecture of individual parietal areas in the monkey (Macaca mulatto) and the distribution of the efferent fibers. Journal of Comparative Neurology 77, 693–737.CrossRefGoogle Scholar
Peterson, B.W., Anderson, M.E. & Filion, M. (1974). Responses of pontomedullary reticular neurons to cortical, tectal and cutaneous stimuli. Experimental Brain Research 21, 19–44.CrossRefGoogle ScholarPubMed
Peterson, B.W., Pitts, N.G., Fukushima, K. & Mackel, R. (1978). Reticulospinal excitation and inhibition of neck motoneurons. Experimental Brain Research 32, 471–489.CrossRefGoogle ScholarPubMed
Porter, J.D., Burns, L.A. & May, P.J. (1989). Morphological substrate for eyelid movements: innervation and structure of primate levator palpebrae superioris and orbicularis oculi muscles. Journal of Comparative Neurology 287, 64–81.CrossRefGoogle ScholarPubMed
Qvist, H. & Dietrichs, E. (1985). The projection from the superior colliculus to the lateral reticular nucleus in the cat as studied with retrograde transport of WGA-HRP. Anatomy and Embryology 173, 269–274.CrossRefGoogle Scholar
Raczkowski, D., Casagrande, V.A. & Diamond, I.T. (1976). Visual neglect in the tree shrew after interruption of the descending projections of the deep superior colliculus. Experimental Neurology 50, 14–29.CrossRefGoogle ScholarPubMed
Raczkowski, D. & Diamond, I.T. (1978). Cells of origin of several efferent pathways from the superior colliculus in Galago senegalensis. Brain Research 146, 351–357.CrossRefGoogle ScholarPubMed
Redgrave, P., Dean, P. & Westby, G.W.M. (1990). Organization of the crossed tecto-reticulo-spinal projection in rat – I. Anatomical evidence for separate output channels to the periabducens area and caudal medulla. Neuroscience 37, 571–584.CrossRefGoogle Scholar
Redgrave, P., Odekunle, A. & Dean, P. (1986). Tectal cells of origin of predorsal bundle in rat: location and segregation from ipsilateral descending pathway. Experimental Brain Research 63, 279–293.CrossRefGoogle ScholarPubMed
Rhoades, R.W. & Dellacroce, D.R. (1980). Cells of origin of the tectospinal tract in the golden hamster: an anatomical and electrophysiological investigation. Experimental Neurology 67, 163–180.CrossRefGoogle ScholarPubMed
Roucoux, A., Guitton, D. & Crommelinck, M. (1980). Stimulation of the superior colliculus in the alert cat. II. Eye and head movements evoked when the head is unrestrained. Experimental Brain Research 39, 75–85.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Koerner, K. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 34, 920–936.CrossRefGoogle ScholarPubMed
Segraves, M.A. & Goldberg, M.E. (1987). Functional properties of corticotectal neurons in the monkey's frontal eye field. Journal of Neurophysiology 58, 1387–1419.CrossRefGoogle ScholarPubMed
Segraves, M.A. & Goldberg, M.E. (1991). Properties of eye and head movements evoked by electrical stimulation of the monkey superior colliculus. In Neuronal Mechanisms of Head-Neck Movement System, ed. Berthoz, A., Graf, W. & Vidal, P.-P. Chap. 46. London: Oxford University Press.Google Scholar
Selemon, L.D. & Goldman-Rakic, P.S. (1988). Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. Journal of Neuroscience 8, 4049–4068.CrossRefGoogle ScholarPubMed
Shook, B.L., Schlag-Rey, M. & Schlag, J. (1990). Primate supplemental eye field: I. Comparative aspects of mesencephalic and pontine connections. Journal of Comparative Neurology 301, 618–642.CrossRefGoogle Scholar
Snider, R.S. & Lee, J.C. (1961). A Stereotaxic Atlas of the Monkey Brain (Macaca mulatto). Chicago: University of Chicago Press.Google Scholar
Sparks, D.L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiological Reviews 66, 118–170.CrossRefGoogle ScholarPubMed
Sparks, D.L. & Hartwich-Young, R. (1989). The deep layers of the superior colliculus. In The Neurobiology of Saccadic Eye Movements. Reviews of Oculomotor Research, Vol. 3, ed. Wurtz, R. & Goldberg, M.E., p. 213–256. Amsterdam: Elsevier Science.Google Scholar
Sparks, D.L. & Mays, L.E. (1983). Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. Journal of Neurophysiology 49, 45–63.CrossRefGoogle ScholarPubMed
Sparks, D.L. & Porter, J.D. (1983). Spatial localization of saccade targets. II. Activity of superior colliculus neurons preceding compensatory saccades. Journal of Neurophysiology 49, 64–74.CrossRefGoogle ScholarPubMed
Stanton, G.B., Goldberg, M.E. & Bruce, C.J. (1988). Frontal eye field efferents in the macaque monkey: II. Topography of terminal fields in midbrain and pons. Journal of Comparative Neurology 271, 493–506.CrossRefGoogle ScholarPubMed
Szabo, J. & Cowan, W.M. (1984). A stereotaxic atlas of the brain of the cynomologous monkey (Macaca fascicularis). Journal of Comparative Neurology 222, 265–300.CrossRefGoogle Scholar
Tehovnik, E.J. (1989). Head and body movements evoked electrically from the caudal superior colliculus of rats: pulse frequency effects. Behavioral Brain Research 34, 71–78.CrossRefGoogle ScholarPubMed
Vidal, P.-P., Corvisier, J. & Berthoz, A. (1983). Eye and neck motor signals in periabducens reticular neurons of the alert cat. Experimental Brain Research 53, 16–28.CrossRefGoogle ScholarPubMed
Vidal, P.-P., May, P.J. & Baker, R. (1988). Synaptic organization of the tectal-facial pathways in the cat. I. Synaptic potentials following collicular stimulation. Journal of Neurophysiology 60, 769–797.CrossRefGoogle ScholarPubMed
Viktorov, I.V. (1966). Neuronal structure of the anterior corpora bigemina of insectivores and rodents. Arkhives D Anatomie, D Gistoligie et D Embriologie 51, 82–89.Google Scholar
Viktorov, I.V. (1968). Neuronal structures of the superior colliculus of the corpora quadrigemina in cat. Arkhives D Anatomie, D Gistoligie et D Embriologie 54, 45–55.Google Scholar
Wallace, M.N. (1988). Lattices of high histochemical activity occur in the human, monkey, and cat superior colliculus. Neuroscience 25, 569–583.CrossRefGoogle ScholarPubMed
Weber, J.T., Martin, G.F., Behan, M., Huerta, M.F. & Harting, J.K. (1979). The origin of the tectospinal pathway in three common laboratory animals: a study using the horseradish peroxidase method. Neuroscience Letters 11, 121–127.CrossRefGoogle ScholarPubMed
Weber, J.T., Partlow, G.D. & Harting, J.K. (1978). The projection of the superior colliculus upon the inferior olivary complex of the cat: an autoradiographic and horseradish peroxidase study. Brain Research 144, 369–377.CrossRefGoogle Scholar
Wiener, S.I. (1986). Laminar distribution and patchiness of cytochrome oxidase in mouse superior colliculus. Journal of Comparative Neurology 244, 137–148.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Albano, J.E. (1980). Visual-motor function of the primate superior colliculus. Annual Reviews of Neuroscience 3, 189–226.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, 575–586.CrossRefGoogle Scholar