Hostname: page-component-586b7cd67f-dsjbd Total loading time: 0 Render date: 2024-11-27T21:14:34.068Z Has data issue: false hasContentIssue false

Pontine projection from striate and prestriate visual cortex in the macaque monkey: An anterograde study

Published online by Cambridge University Press:  02 June 2009

W. Fries
Affiliation:
Neurologische Klinik and Institut fÜr Medizinische Psychologie, Universität MÜnchen, FRG

Abstract

The projection from striate and prestriate visual cortex to the pontine nuclei has been studied in the macaque monkey by means of anterograde tracer techniques in order to assess the contribution of anatomically and functionally distinct visual cortical areas to the cortico-ponto-cerebellar loop. No projection to the pons was found from central or paracentral visual-field representations of V1 (striate cortex) or prestriate visual areas V2, and V4. Small patches of terminal labeling occurred after injections of tracer into more peripheral parts of V1, V2 and V3, and into V3A. The terminal fields were located most dorsolaterally in the anterior to middle third of the pons and were quite restricted in their rostro-caudal extent. Injections of V5, however, yielded substantial terminal labeling, stretching longitudinally throughout almost the entire pons. This projection could be demonstrated to arise from parts of V5 receiving input from central visual-field representations of striate cortex, whereas parts of V4 receiving similarly central visual-field input had no detectable projection to the pons. Its distribution may overlap to a large extent with the termination of tecto-pontine fibers and with the termination of fibers from visual areas in the medial bank (area V6 or P0) and lateral bank (area LIP) of the intraparietal sulcus, as well as from frontal eye fields (FEF). It appears that the main information relayed to the cerebellum by the visual corticopontine projection is related to movement in the field of view.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 1990

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

Adams, J.C. (1980). Stabilizing and rapid thionin staining of TMB based HRP reaction product. Neuroscience Letters 17, 79.Google Scholar
Albright, T.D. & Desimone, B. (1987). Local precision of visuotopic organization in the middle temporal area (MT) of the macaque. Experimental Brain Research 65, 582592.CrossRefGoogle ScholarPubMed
Albus, K., Donate-Oliver, F., Sanides, D. & Fries, W. (1981). The distribution of pontine projection cells in visual and association cortex of the cat: an experimental study with HRP. Journal of Comparative Neurology 201, 175189.CrossRefGoogle Scholar
Aschoff, J.C. (1974). Reconsideration of the oculomotor pathway. In The Neurosciences, Vol. III: Study Program, ed Schmitt, F.O. & Worden, F.G., pp. 305310. Cambridge Massachusetts and London, UK: MIT Press.Google Scholar
Baker, J., Gibson, A., Glickstein, M. & Stein, J. (1976). Visual cells in the pontine nuclei of cat. Journal of Physiology 225, 415433.CrossRefGoogle Scholar
Brodal, P. (1972 a). The corticopontine projection from the visual cortex in the cat, I: The total projection and the projection from area 17. Brain Research 39, 297317.CrossRefGoogle ScholarPubMed
Brodal, P. (1972 b) The corticopontine projection from the visual cortex in the cat, II: The projection from areas 18 and 19. Brain Research 39, 319355.CrossRefGoogle ScholarPubMed
Brodal, P. (1978). The corticopontine projection in the rhesus monkey: origin and prinicples of organization. Brain 101, 251283.CrossRefGoogle Scholar
Brodal, P. (1979). The ponto-cerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193208.CrossRefGoogle Scholar
Brodmann, K. (1905). Beiträge zur histologischen Lokalisation der Grosshirnrinde. J. Psychol. Neurol. Lpz. 4, 177226.Google Scholar
Bruce, C.J., Desimone, R. & Gross, C.G. (1981). Visual properties in a polysensory area in superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 269384.CrossRefGoogle Scholar
Colby, C.L., Gattass, R., Olson, C.R. & Gross, C.G. (1988). Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. Journal of Comparative Neurology 269, 392413.CrossRefGoogle ScholarPubMed
Cowan, W.M., Gottlieb, D.J., Hendrickson, A.E., Price, J.L. & Woolsey, T. A. (1972). The autoradiographic demonstration of axonal connection in the central nervous system. Brain Research 37, 2151.Google Scholar
Cynader, M. & Berman, M. (1972). Receptive-field organization of monkey superior colliculus. Journal of Neurophysiology 35, 187201.CrossRefGoogle ScholarPubMed
Daniel, P.M. & Whitteridge, D. (1961). The representation of the visual field on the cerebral cortex in monkeys. Journal of Physiology 159, 203221.CrossRefGoogle ScholarPubMed
Dichgans, J. & Jung, R. (1975). Oculomotor abnormalities due to cerebellar lesions. In Basic Mechanisms of Ocular Motility and Their Clinical Implications, ed. Lennerstrand, G. & Bach-y-Rita, P. pp. 281298. Oxford: Pergamon Press.Google Scholar
Dieterich, M. & Brandt, Th. (1987). Impaired motion perception in congenital nystagmus and acquired oculomotor palsy. Clinical Vision Science 1, 337345.Google Scholar
Eckmiller, R. & Westheimer, G. (1983). Compensation of oculomotor deficits in monkeys with neonatal cerebellar ablations. Experimental Brain Research 49, 315326.Google Scholar
Faugier-Grimaud, S. & Ventre, J. (1989). Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo-ocular function in a monkey (Macaca fascicularis). Journal of Comparative Neurology 280, 114.Google Scholar
Felix, D. & KÜnzle, H. (1974). Iontophoretic and autoradiographic studies on the role of proline in nervous transmission.PflÜgers Archiv 350, 135144.Google Scholar
Fries, W. (1981). The projection from striate and prestriate visual cortex onto the pontine nuclei of the macaque monkey. Society of Neuroscience Abstracts 7, 762.Google Scholar
Fries, W. (1984). Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. Journal of Comparative Neurology 230, 5576.CrossRefGoogle Scholar
Fries, W. & Albus, K. (1980). Responses of pontine nuclei cells to electrical stimulation of the lateral and suprasylvaian gyrus in the cat. Brain Research 188, 255260.Google Scholar
Fries, W. & Zeki, S. (1983 a). The laminar origin of the cortical inputs to the fourth visual complex of macaque monkey. Journal of Physiology 342, 57P.Google Scholar
Fries, W. & Zeki, S. (1983 b). Laminar origin of cortical inputs into macaque prestriate visual cortex. Little evidence for a single rule. Neuroscience Letters (Suppl.) 14, 122.Google Scholar
Gattass, R. & Gross, C.G. (1981). Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. Journal of Neurophysiology 46, 621638.Google Scholar
Gattass, R., Sousa, A.P.B. & Gross, C.G. (1988). Visuotopic organization and extent of V3 and V4 of the macaque. Journal of Neuroscience 8, 18311845.CrossRefGoogle ScholarPubMed
Glickstein, M., Cohen, J.L., Dixon, B., Gibson, A., Hollins, M., Labossiere, E. & Robinson, F. (1980). Corticopontine visual projections in macaque monkeys. Journal of Comparative Neurology 190, 521541.Google ScholarPubMed
Glickstein, M., Stein, J. & King, R. (1972). Visual input to the pontine nuclei. Science 178, 11101111.Google Scholar
Glickstein, M., May, J.G. & Mercier, B.E. (1985). Corticopontine projection in the macaque: the distribution of labeled cortical cells after large injections of horseradish peroxidase in the pontine nuclei. Journal of Comparative Neurology 235, 343359.Google Scholar
Harting, J.K. (1977). Descending pathways from superior colliculus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). Journal of Comparative Neurology 173, 583612.Google Scholar
Huerta, M.F., Krubitzer, L. & Kaas, J.H. (1988). Frontal eye fields as defined by intracortical microstimulation squirrel monkeys, owl monkeys, and macaque monkeys, I: Subcortical connections. Journal of Comparative Neurology 253, 415439.CrossRefGoogle Scholar
KÜnzie, H. & Akert, K. (1977). Efferent connections of cortical area 8 (frontal eye fields) in Macaca fascicularis. A reinvestigation using the autoradiographic technique. Journal of Comparative Neurology 173, 147164.Google Scholar
Leichnetz, G.R., Smith, D.J. & Spencer, R.F. (1984). Cortical projections to the paramedian tegmental and basilar pons in the monkey. Journal of Comparative Neurology 228, 388408.CrossRefGoogle Scholar
Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.E. & Fuchs, A.F. (1975). The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 164, 287304.CrossRefGoogle ScholarPubMed
Lynch, G.C. (1987). Frontal eye-field lesions in monkeys disrupt visual pursuit. Experimental Brain Research 68, 437441.CrossRefGoogle ScholarPubMed
Lynch, G.C., Mountcastle, V.B., Talbot, W.H. & Yin, T.C.T. (1977). Parietal lob mechanisms for directed visual attention. Journal of Neurophysiology 40, 362389.Google Scholar
Maunsell, J.H.R. & Van, Essen D.C. (1983). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 25632586.Google Scholar
May, J.G., & Andersen, R.A. (1986). Different patterns of corticopontine projections from separate cortical fields within the inferior parietal lobule and dorsal prelunate gyrus of the macaque. Experimental Brain Research 63, 265278.CrossRefGoogle ScholarPubMed
May, J.G., Keller, E.L. & Suzuki, D.A. (1988). Smooth-pursuit eye movement deficits with chemical lesions in the dorsolateral pontine nucleus of the monkey. Journal of Neurophysiology 59, 952977.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1978). Tetramethylbenzidine for horseradish peroxidase neurohistochemistry: a noncarcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and effereents. Journal of Histochemistry and Cytochemistry 26, 106117.Google Scholar
Mohler, C.W., Goldberg, M.E. & Wurtz, R.H. (1973). Visual receptive fields of frontal eye-field neurons. Brain Research 61, 385389.CrossRefGoogle ScholarPubMed
Mustari, M.J., Fuchs, A.F. & Wallman, J. (1988). Response properties of dorsolateral pontine units during smooth pursuit in the rhesus monkey. Journal of Neurophysiology 60, 664686.CrossRefGoogle Scholar
Noda, H. & Suzuki, D.A. (1979). The role of the flocculus in fixation and smooth-pursuit eye movements. Journal of Physiology 294, 335348.CrossRefGoogle ScholarPubMed
Nyby, O. & Jansen, J. (1951). An experimental investigation of the corticopontine projection in macaca mulatta. Norske Videnskaps-Akademi Oslo, I, Matematisk-Naturvideanskapelig Klasse: Avhandlinger 3, 147.Google Scholar
Rashbass, C. (1961). The relationship between saccadic and smoothtracking eye movements. Journal of Physiology 159, 326338.CrossRefGoogle ScholarPubMed
Ritchie, C. (1976). Effects of cerebellar lesions on saccadic eye movements. Journal of Neurophysiology 39, 12461256.CrossRefGoogle ScholarPubMed
Rizzolatti, G., Scandorla, C., Matelli, M. & Gentilucci, M. (1981). Afferent properties of periarcuate neurons in macaque monkeys, II: Visual responses. Behavioral Brain Research 2, 147163.CrossRefGoogle ScholarPubMed
Sakata, H., Shibutani, H. & Kawanko, K. (1983). Functional properties of visual-tracking neurons in posterior parietal association cortex of the monkey. Journal of Neurophysiology 49, 13641380.Google Scholar
Sanides, D., Fries, W. & Albus, K. (1978) The cortico-pontine projection from the visual cortex of the cat: an autoradiographic investigation. Journal of Comparative Neurology 179, 7788.Google Scholar
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. Journal of Neurophysiology 34, 920936.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, 493506.CrossRefGoogle ScholarPubMed
Stein, J.F. (1986). Role of the cerebellum in the visual guidance of movement. Nature 323, 217221.Google Scholar
Sunderland, S. (1940). The projection of the cerebral cortex on the pons and cerebellum in the macaque monkey. Journal of Anatomy (London) 74, 201226.Google ScholarPubMed
Suzuki, D.A. & Keller, E.L. (1984). Visual signals in the dorsolateral pontine nucleus of the alert monkey: their relationship to smooth- pursuit eye movements. Experimental Brain Research 53, 473478.CrossRefGoogle ScholarPubMed
Suzuki, D.A., Noda, H. & Kase, M. (1981). Visual and pursuit eye movement-related activity in posterior vermis of monkey cerebellum. Journal of Neurophysiology 46, 11201139.CrossRefGoogle ScholarPubMed
Thier, P., Koehler, W. & Buettner, U.W. (1988). Neuronal activity in the dorsolateral pontine nucleus of the alert monkey modulated by visual stimuli and eye movements. Experimental Brain Research 70, 496512.Google Scholar
Tusa, R.J. & Ungerleider, L.G. (1988). Fiber pathways of cortical areas mediating smooth-pursuit eye movements in monkeys. Annals of Neurology 23, 174183.Google Scholar
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 284, 190222.Google Scholar
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection zone in the temporal sulcus of Macaca mulatta: location and topographic organization. Journal of Comparative Neurology 188, 347366.Google Scholar
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984). Subcortical projections of area MT in macaque. Journal of Comparative Neurology 223, 368386.Google Scholar
Vanegas, H., Hollander, H. & Distel, H. (1978). Early stages of uptake and transport of horseradish peroxidase by cortical strictures, and its use for the study of local neurons and their processes. Journal of Comparative Neurology 177, 193212.CrossRefGoogle Scholar
Van, Essen D.C., Maunsell, J.H.R. & Bixby, J.L. (1981). The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties, and topographic representation. Journal of Comparative Neurology 199, 293326.Google Scholar
Van, Eaaen D.C. & Zeki, S.M. (1978). The topographic organization of rhesus monkey prestriate cortex. Journal of Physiology 277, 193226.Google Scholar
Westheimer, G. & Blair, S.M. (1974). Functional organization of primate oculomotor system revealed by cerebellectomy. Experimental Brain Research 21, 463472.CrossRefGoogle ScholarPubMed
Wiesendanger, R., Wiesendanger, M. & Ruegg, D.G. (1979). An anatomical investigation of the corticopontine projection in the primate (Macaca fascicularis and Saimiri sciureus), II: The projection from frontal and parietal association areas. Neuroscience 4, 747765.Google Scholar
Yamada, J. & Noda, H. (1987). Afferent and efferent connections of he oculomotor cerebellar vermis in the macaque monkey. Journal of Comparative Neurology 265, 224241.Google Scholar
Zeki, S.M. (1970). Interhemispheric connections of prestriate cortex in monkey. Brain Research 19, 6375.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus in the rhesus monkey. Journal of Physiology 236, 549573.Google Scholar
Zeki, S.M. (1977). Colour coding in the superior temporal sulcus of rhesus monkey visual cortex. Proceedings of the Royal Society B (London) 197, 195223.Google Scholar
Zeki, S.M. (1978 a). Functional specialisation in the visual cortex of the rhesus monkey. Nature 274, 423428.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1978 b). Uniformity and diversity of structure and function in rhesus monkey prestriate cortex. Journal of Physiology 277, 273290.CrossRefGoogle Scholar
Zeki, S.M. (1980). Representation of colour in the cerebral cortex. Nature 284, 412418.Google Scholar
Zeki, S. (1986). The anatomy and physiology of area V6 of macaque monkey visual cortex. Journal of Physiology 381, 62P.Google Scholar