Hostname: page-component-586b7cd67f-l7hp2 Total loading time: 0 Render date: 2024-11-23T09:46:42.699Z Has data issue: false hasContentIssue false
  • English
  • Français

Inferior frontal eye field projections to the pursuit-related dorsolateral pontine nucleus and middle temporal area (MT) in the monkey

Published online by Cambridge University Press:  02 June 2009

George R. Leichnetz
George R. Leichnetz*
Affiliation:
Department of Anatomy, Medical College of Virginia, Virginia Commonwealth University, Richmond
*
Correspondence and reprint requests to: George R. Leichnetz, Department of Anatomy, Box 709, Medical College of Virginia, Virginia Commonwealth University, Richmond, VA 23298-0709, USA.
Get access Rights & Permissions [Opens in a new window]

Abstract

Inferior frontal eye field (FEF) projections to the dorsolateral pontine nucleus (DLPN), and corticocortical connections with the superior temporal sulcal (STS) cortex, were studied in five macaque monkeys which had received horseradish peroxidase (HRP) gel implants into the inferior prearcuate cortex (including area 45 of Walker, 1940). These connections were contrasted with those from the dorsal FEF (area 8a) in another macaque monkey. Findings of heavy inferior FEF projections to the ipsilateral DLPN (light to the contralateral DLPN) and reciprocal connections with the deep caudal bank and fundus of the superior temporal sulcus (STS), presumed to be the middle temporal (MT) visual area (Maunsell & Van Essen, 1983a), appeared to go hand in hand with more pronounced projections to the stratum superficialis of the superior colliculus (SC). In contrast, the HRP gel implant in the dorsal prearcuate cortex (area 8a of Walker, 1940) resulted in only very light projections to the ipsilateral DLPN, more pronounced projections to the dorsomedial pontine nucleus (DMPN), almost no projection to the stratum superficialis (SS), and more pronounced reciprocal connections with the upper bank of the STS, presumed to be the medial superior temporal (MST) area (Maunsell & Van Essen, 1983a). Both the inferior and dorsal FEF also had extensive reciprocal connections with the ventral intraparietal area (VIP; Maunsell & Van Essen, 1983a) in the caudal bank of the intraparietal sulcus. The correlated projections of the inferior FEF to the DLPN, MT area, and SS may explain its reported role in smooth pursuit (Lynch, 1987), in addition to its well-established role in the production of voluntary purposeful saccadic eye movements (Bruce et al., 1985).

Keywords

Smooth pursuitSaccadic and slow eye movementsFixationArea 8Middle temporal (MT) areaMedial superior temporal (MST) areaSuperior colliculus
Type
Research Articles
Information
Visual Neuroscience , Volume 3 , Issue 2 , August 1989 , pp. 171 - 180
Copyright
Copyright © Cambridge University Press 1989

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

Albright, T.D., Desimone, R. & Gross, C.G. (1984). Columnar organization of directionally selective cells in visual area MT of the macaque. Journal of Neurophysiology 51, 16–31.CrossRefGoogle ScholarPubMed
Barbas, H. & Mesulam, M.M. (1981). Organization of afferent input to subdivisions of area 8 in the rhesus monkey. Journal of Comparative Neurology 200, 407–431.CrossRefGoogle ScholarPubMed
Brodal, P. (1982). Further observations on the cerebellar projections from the pontine nuclei and the nucleus reticularis tegmenti pontis in the rhesus monkey. Journal of Comparative Neurology 204, 44–45.CrossRefGoogle ScholarPubMed
Bruce, C.J., Goldberg, M.E., Bushnell, M.C. & Stanton, G.B. (1985). Primate frontal eye fields, II: Physiological and anatomical correlates of electrically evoked eye movements. Journal of Neurophysiology 54, 714–734.CrossRefGoogle ScholarPubMed
Bushnell, M.C, Goldberg, M.E. & Robinson, D.L. (1981). Behavioral enhancement of visual responses in monkey cerebral cortex, I: Modulation in posterior parietal cortex related to selective visual attention. Journal of Neurophysiology 46, 755–772.CrossRefGoogle ScholarPubMed
Casagrande, V.A. & Harting, J.K. (1975). Transneuronal transport of tritiated fucose and proline in the visual system of the tree shrew (Tupaia glis). Brain Research 96, 367–372.CrossRefGoogle Scholar
Collewijn, H., Curio, G. & Grüsser, O.J. (1982). Spatially selective visual attention and generation of eye pursuit movements. Human Neurobiology 1, 129–139.Google ScholarPubMed
Desimone, R. & Ungerleider, L.G. (1986). Multiple visual areas in the caudal superior temporal sulcus of the macaque. Journal of Comparative Neurology 248, 164–189.CrossRefGoogle ScholarPubMed
Dürsteler, M.R., Wurtz, R.H. & Newsome, W.T. (1987). Directional pursuit deficits following lesions of the foveal representation within the superior temporal sulcus of the macaque monkey. Journal of Neurophysiology 51, 1262–1287.CrossRefGoogle Scholar
Eckmiller, R. (1987). Neural control of pursuit eye movements. Physiological Reviews 67, 797–857.CrossRefGoogle ScholarPubMed
Eckmiller, R. & Mackeben, M. (1978). Pursuit eye movements and their neural control in the monkey. Pfluegers Archiv 377, 15–23.CrossRefGoogle ScholarPubMed
Fries, W. (1984). Cortical projections to the superior colliculus in the macaque monkey: a retrograde study using horseradish peroxidase. Journal of Comparative Neurology 230, 55–76.CrossRefGoogle Scholar
Giolli, R.A., Blanks, R.H.I. & Torigoe, Y. (1984). Pretectal and brain stem projections of the medial terminal nucleus of the accessory optic system of the rabbit and rat as studied by anterograde and retrograde neuronal tracing methods. Journal of Comparative Neurology 227, 228–251.CrossRefGoogle ScholarPubMed
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, 343–359.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, 209–229.CrossRefGoogle ScholarPubMed
Goldberg, M.E. & Wurtz, R.H. (1971). Response of single cells in monkey superior colliculus during pursuit eye movement and stationary fixation. Neurology 21, 435.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
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
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., 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
Huerta, M.F., Casagrande, V.A., Weber, J.T. & Harting, J.K. (1976). Transneuronal transport of 3H proline within the visual system of the grey squirrel. Society for Neuroscience Abstracts 2(1549), 1078.Google Scholar
Ito, M. (1982). Eye movements and the cerebellum. In The Cerebellum: New Vistas, ed. Palay, S.L., Chan-Palay, V., pp. 515–532. Berlin: Springer-Verlag.CrossRefGoogle Scholar
Kase, M., Miller, D.C. & Noda, H. (1980). Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation. Journal of Physiology (London) 300, 539–555.CrossRefGoogle ScholarPubMed
Kawano, K., Sasaki, M. & Yamashita, M. (1984). Response properties of neurons in posterior parietal cortex of monkey during visual-vestibular stimulation, I: Visual tracking neurons. Journal of Neu-rophysiology 51, 340–351.Google ScholarPubMed
Komatsu, H. & Suzuki, H. (1985). Projections from the functional subdivisions of the frontal eye field to the superior colliculus in the monkey. Brain Research 327, 324–327.CrossRefGoogle Scholar
Komatsu, H. & Wurtz, R.H. (1988). Relation of cortical areas MT and MST to pursuit eye movements, I: Localization and visual properties of neurons. Journal of Neurophysiology 60, 580–603.CrossRefGoogle ScholarPubMed
Künzle, 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., Fuchs, A.F., Scudder, C.A. & Chubb, M.C. (1985). Afferents to the flocculus of the cerebellum in the rhesus macaque as revealed by retrograde transport of horseradish peroxidase. Journal of Comparative Neurology 235, 1–25.CrossRefGoogle Scholar
Leichnetz, G.R. & Gonzalo-Ruiz, A. (1988). Oculomotor-related connections of the cerebellar fastigial nucleus in the monkey, and their relationship to frontal eye field efferents. Society for Neuroscience Abstracts 14(248.3), 611.Google 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, ed. Burr-Ner-Ennever, J.A., pp. 365–429. Amsterdam: Elsevier-North Holland.Google Scholar
Leichnetz, G.R., Spencer, R.F., Hardy, S.G.P. & Astruc, J.A. (1981). The prefrontal corticotectal projection in the monkey: an an-terograde and retrograde horseradish peroxidase study. Neuroscience 6, 1023–1041.CrossRefGoogle ScholarPubMed
Leichnetz, G.R., Spencer, R.F. & Smith, D.J. (1984 a). Cortical projections to nuclei adjacent to the oculomotor complex in the medial dien-mesencephalic tegmentum in the monkey. Journal of Comparative Neurology 228, 359–387.CrossRefGoogle Scholar
Leichnetz, G.R., Smith, D.J. & Spencer, R.F. (1984 b). Cortical projections to the paramedian tegmental and basilar pons in the monkey. Journal of Comparative Neurology 228, 388–408.CrossRefGoogle Scholar
Levin, S. (1984). Frontal lobe dysfunctions in schizophrenia, I: Eye movement impairments. Journal of Psychiatric Research 18, 27–55.CrossRefGoogle ScholarPubMed
Lisberger, S.G., Morris, E.J. & Tychsen, L. (1987). Visual motion processing and sensory-motor integration for smooth-pursuit eye movements. Annual Review of Neuroscience 10, 97–129.CrossRefGoogle ScholarPubMed
Lynch, J.C. (1987). Frontal eye field lesions in monkeys disrupt visual pursuit. Experimental Brain Research 68, 437–441.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
Lynch, J.C, Mountcastle, V.B., Talbot, W.H. & Yin, T.C.T. (1977). Parietal lobe mechanisms for directed visual attention. Journal of Neurophysiology 40, 362–389.CrossRefGoogle ScholarPubMed
MacAvoy, M.C, Bruce, C.J. & Gottlieb, J. (1988). Smooth-pursuit eye movements elicited by microstimulation in the frontal eye fields region of alert macaque monkeys. Society for Neuroscience Abstracts 386 (9), 956.Google Scholar
Maioli, M.G., Squatrito, S., Galletti, C, Battaglini, P.P. & San-Serverino, E.R. (1983). Corticocortical connections from the visual region of the superior temporal sulcus to frontal eye field in the macaque. Brain Research 265, 294–299.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Essen, D.C.Van (1983 a). The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. Journal of Neuroscience 3, 2563–2586.CrossRefGoogle ScholarPubMed
Maunsell, J.H.R. & Essen, D.C.Van (1983 b). Functional properties of neurons in middle temporal area of the macaque monkey, I: Selectivity for stimulus direction, speed, and orientation. Journal of Neurophysiology 49, 1127–1147.CrossRefGoogle ScholarPubMed
May, J.G., Keller, E.L. & Crandall, W.F. (1985). Changes in eye velocity during smooth-pursuit tracking induced by microstimulation of the dorsolateral pontine nucleus of the macaque. Society for Neuroscience Abstracts 11(25.12), 79.Google Scholar
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, 952–975.CrossRefGoogle ScholarPubMed
McElligott, J.G. & Keller, E.L. (1984). Cerebellar vermis involvement in monkey saccadic eye movements: microstimulation. Experimental Neurology 86, 543–558.CrossRefGoogle ScholarPubMed
Mesulam, M.M. (1978). A tetramethylbenzidine method for the light microscopic tracing of neural connections with horseradish peroxidase (HRP) neurohistochemistry. In Neuroanatomical Techniques, Short Course, pp. 65–71. Bethesda: Society for Neuroscience.Google Scholar
Mower, G., Gibson, A. & Glickstein, M. (1979). Tectopontine pathway in the cat: laminar distribution of cells of origin and visual properties of target cells in dorsolateral pontine nucleus. Journal of Neurophysiology 42, 1–15.CrossRefGoogle ScholarPubMed
Munoz, D.P. & Guitton, D. (1988). Rostral output neurons of superior colliculus are active during attentive fixation. Society for Neuroscience Abstracts 14(386.6), 956.Google Scholar
Mustari, M.J., Fuchs, A.F. & Wallman, J. (1988). Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. Journal of Neurophysiology 60, 664–686.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H., Dürsteler, M.R. & Mikami, A. (1985). Deficits in visual motion processing following ibotemic-acid lesions of the middle temporal visual area of the macaque monkey. Journal of Neuroscience 5, 825–840.CrossRefGoogle ScholarPubMed
Noda, H. & Fujikado, T. (1987). Topography of the oculomotor area of the cerebellar vermis in macaques as determined by microstimulation. Journal of Neurophysiology 58, 359–378.CrossRefGoogle ScholarPubMed
Noda, H.Murakami, S., Yamada, J., Tamaki, Y. & Aso, T. (1988). Saccadic eye movements evoked by microstimulation of the fastigial nucleus of macaque monkeys. Journal of Neurophysiology 60, 1036–1052.CrossRefGoogle ScholarPubMed
Nyby, O. & Jansen, J. (1951). An experimental investigation of the corticopontine projection in Macaca Mulatta. Norske Videnskaps-Akademi, Avh. I, Mat.-Naturv. Klasse 3, 1–47.Google Scholar
Robinson, D.L., Goldberg, M.E. & Stanton, G.B. (1978). Parietal association cortex in the primate: sensory mechanisms and behavioral modulations. Journal of Neurophysiology 41, 910–932.CrossRefGoogle ScholarPubMed
Ron, S. & Robinson, D.A. (1973). Eye Movements evoked by cerebellar stimulation in the alert monkey. Journal of Neurophysiology 36, 1004–1022.CrossRefGoogle ScholarPubMed
Schiller, P.H. & Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert monkey. Journal of Neurophysiology 34, 920–936.CrossRefGoogle Scholar
Segraves, M.A. & Goldberg, M.E. (1987). Functional properties of corticotectal neurons in the monkey's frontal eye field. Journal of Neurophysiology 18, 1387–1419.CrossRefGoogle Scholar
Seltzer, B. & Pandya, D.N. (1978). Afferent connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research 149, 1–24.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
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, 1120–1134.CrossRefGoogle 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, 473–478.CrossRefGoogle ScholarPubMed
Suzuki, D.A., May, J. & Keller, E.L. (1984). Smooth-pursuit eye movement deficits with pharmacological lesions in monkey dorsolateral pontine nucleus. Society for Neuroscience Abstracts 10(21.3), 58.Google Scholar
Suzuki, D.A. & Keller, E.L. (1988). The role of the posterior vermis of monkey cerebellum in smooth-pursuit eye movement control, I: Eye and head movement-related activity. Journal of Neurophysiology 59, 1–18.CrossRefGoogle ScholarPubMed
Thier, R., 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, 496–512.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Comparative Neurology 248, 190–222.CrossRefGoogle ScholarPubMed
Ungerleider, L.G. & Mishkin, M. (1979). The striate projection zone in the superior temporal sulcus of Macaca mulatto: location and topographic organization. Journal of Comparative Neurology 188, 347–366.CrossRefGoogle Scholar
Ungerleider, L.G., Desimone, R., Galkin, T.W. & Mishkin, M. (1984). Subcortical projections of area MT in the macaque. Journal of Comparative Neurology 232, 368–386.CrossRefGoogle Scholar
Essen, D.C.Van, Maunsell, J.H.R. & Bixby, J.L. (1981). The Middle temporal visual area in the macaque: myeloarchitecture, connective, functional properties, and topographical connections. Journal of Comparative Neurology 199, 293–326.CrossRefGoogle Scholar
Walker, A.E. (1940). A cytoarchitectural study of the prefrontal area of the macaque monkey. Journal of Comparative Neurology 73, 59–86.CrossRefGoogle Scholar
Weber, J.T. & Harting, J.K. (1980). The efferent projections of the pretectal complex: an autoradiographic and horseradish peroxidase analysis. Brain Research 194, 1–28.CrossRefGoogle ScholarPubMed
Wurtz, R.H. & Albano, J.E. (1980). Visual-motor function of the primate superior collkulus. Annual Review of Neuroscience 3, 189–226.CrossRefGoogle Scholar
Yamada, J. & Noda, H. (1987). Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. Journal of Comparative Neurology 265, 224–241.CrossRefGoogle ScholarPubMed
Zee, D.S., Yamazaki, A., Butler, P.H. & Gucer, G. (1981). Effects of ablation of flocculus and paraflocculus on eye movements in primate. Journal of Neurophysiology 46, 878–899.CrossRefGoogle ScholarPubMed
Zeki, S.M. (1974). Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. Journal of Physiology (London) 236, 549–573.CrossRefGoogle ScholarPubMed