Hostname: page-component-78c5997874-8bhkd Total loading time: 0 Render date: 2024-11-10T15:50:45.321Z Has data issue: false hasContentIssue false

Topography of supplementary eye field afferents to frontal eye field in macaque: Implications for mapping between saccade coordinate systems

Published online by Cambridge University Press:  02 June 2009

Jeffrey D. Schall
Affiliation:
Department of Psychology, Wilson Hall, Vanderbilt University, Nashville
Anne Morel
Affiliation:
Neurosurgery Clinic, University Hospital, Rämistrasse 100, CH-8091 Zurich, Switzerland
Jon H. Kaas
Affiliation:
Department of Psychology, Wilson Hall, Vanderbilt University, Nashville

Abstract

Two discrete areas in frontal cortex are involved in generating saccadic eye movements—the frontal eye field (FEF) and the supplementary eye field (SEF). Whereas FEF represents saccades in a topographic retinotopic map, recent evidence indicates that saccades may be represented craniotopically in SEF. To further investigate the relationship between these areas, the topographic organization of afferents to FEF from SEF in Macaco mulatto was examined by placing injections of distinct retrograde tracers into different parts of FEF that represented saccades of different amplitudes. Central FEF (lateral area 8A), which represents saccades of intermediate amplitudes, received afferents from a larger portion of SEF than did lateral FEF (area 45), which represents shorter saccades, or medial FEF (medial area 8A), which represents the longest saccades in addition to pinna movements. Moreover, in every case the zone in SEF that innervated lateral FEF (area 45) also projected to medial FEF (area 8A). In one case, a zone in rostral SEF projected to both lateral area 8A from which eye movements were evoked by microstimulation as well as medial area 8A from which pinna movements were elicited by microstimulation. This pattern of afferent convergence and divergence from SEF onto the retinotopic saccade map in FEF is indicative of some sort of map transformation between SEF and FEF. Such a transformation would be necessary to interconnect a topographic craniotopic saccade representation in SEF with a topographic retinotopic saccade representation in FEF.

Type
Research Article
Copyright
Copyright © Cambridge University Press 1993

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

Andersen, R.A., Bracewell, M., Barash, S., Gnadt, J. & Fogassi, L. (1990). Eye position effects on visual, memory, and saccaderelated activity in areas LIP and 7a of macaque. Journal of Neuroscience 10, 11761196CrossRefGoogle ScholarPubMed
Arikuni, T., Watanabe, K. & Kubota, K. (1988). Connections of area 8 with area 6 in the brain of the macaque monkey. Journal of Comparative Neurology 277, 2140CrossRefGoogle 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, 407431CrossRefGoogle ScholarPubMed
Barbas, H. & Pandya, D.N. (1987). Architecture and frontal cortical connections of the premotor cortex (area 6) in the rhesus monkey. Journal of Comparative Neurology 256, 211228CrossRefGoogle ScholarPubMed
Bruce, C.J. (1990). Integration of sensory and motor signals for saccadic eye movements in the primate frontal eye fields. In Signals and Sense in Cerebral Cortex, ed. Edelman, G.M., Gall, W.E. & Cowan, W.M., pp. 261314. New York: John Wiley and Sons.Google Scholar
Bruce, C.J. & Borden, J.A. (1986). The primate frontal eye fields are necessary for predictive saccadic tracking. Society for Neuroscience Abstracts 12, 1086.Google Scholar
Bruce, C.J. & Goldberg, M.E. (1985). Primate frontal eye fields. I. Single neurons discharging before saccades. Journal of Neurophysiology 53, 603635CrossRefGoogle ScholarPubMed
Bruce, C.J., Goldberg, M.E., Bushnell, C. & Stanton, G.B. (1985). Primate frontal eye fields. II. Physiological and anatomical correlates of electrically evoked eye movements. Journal of Neurophysiology 54, 714734CrossRefGoogle ScholarPubMed
Bruce, C.J. & Russo, G.S. (1987). Effects of ketamine on oculomotor function in the monkey. Society for Neuroscience Abstracts 13, 171.Google Scholar
Burman, D.D., Bruce, C.J. & Russo, G.S. (1988). Pinna movements elicited by microstimulation in the prefrontal cortex of monkeys. Society for Neuroscience Abstracts 14, 208.Google Scholar
Deng, S.-Y., Goldberg, M.E., Segraves, M.A., Ungerleider, L.G. & Mishkin, M. (1986). The effect of unilateral ablation of the frontal eye fields on saccadic performance in the monkey. In Adaptive Processes in Visual and Oculomotor Systems, ed. Keller, E.L. & Zee, D.S., pp. 201208. Oxford: Pergamon.Google Scholar
Galaburda, A.M. & Pandya, D.N. (1983). The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey. Journal of Comparative Neurology 221, 169184CrossRefGoogle ScholarPubMed
Gaymard, B., Pierrot-Deseilligny, C. & Rtvaud, S. (1990). Impairment of sequences of memory-guided saccades after supplementary motor area lesions. Annual Review of Neurology 28, 622626CrossRefGoogle ScholarPubMed
Gibson, A.R., Hansma, D.I., Hour, J.C. & Robinson, F.R. (1984). A sensitive low artifact TMB procedure for the demonstration of WGA-HRP in the CNS. Brain Research 298, 235241CrossRefGoogle ScholarPubMed
Godaux, E., Cheron, G. & Mettens, P. (1990). Ketamine induces failure of the oculomotor neural integrator in the cat. Neuroscience Letters 116, 162167CrossRefGoogle ScholarPubMed
Goldberg, G. (1985). Supplementary motor area structure and function: Review and hypotheses. Behavior and Brain Sciences 8, 567616CrossRefGoogle Scholar
Goldberg, M.E. & Bruce, C.J. (1990). Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. Journal of Neurophysiology 64, 489508CrossRefGoogle ScholarPubMed
Goldberg, M.E. & Segraves, M.A. (1989). Visual and frontal cortices. In The Neurobiology of Saccadic Eye Movements, ed. Wurtz, R.H. & Goldberg, M.E., pp. 283313. New York: Elsevier.Google Scholar
Gould, J.H., Cusick, C.G., Pons, T.P. & Kaas, J.H. (1986). The relationship of corpus callosum connections to electrical stimulation maps of motor, supplementary motor, and frontal eye fields in owl monkeys. Journal of Comparative Neurology 247, 297325CrossRefGoogle ScholarPubMed
Guitton, D., Buchtel, H.A. & Douglas, R.M. (1985). Frontal lobe lesions in man cause difficulties in suppressing reflexive glances and in generating goal-directed saccades. Experimental Brain Research 58, 455472CrossRefGoogle ScholarPubMed
Hallett, P.E. & Lightstone, A.D. (1976). Saccadic eye movements towards stimuli triggered by prior saccades. Vision Research 16, 99106CrossRefGoogle ScholarPubMed
Huerta, M.F. & Kaas, J.H. (1990). Supplementary eye field as defined by intracortical microstimulation: Connections in macaques. Journal of Comparative Neurology 293, 299330CrossRefGoogle ScholarPubMed
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1987). Frontal eye fields as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. Journal of Comparative Neurology 271, 473492Google Scholar
Lee, K.M. & Tehovnik, E.J. (1991). Eye position dependency of units in the dorsomedial frontal cortex. Society for Neuroscience Abstracts 17, 546.Google Scholar
Luppino, G., Matelli, M. & Rizzolatti, G. (1990). Cortico-cortical connections of two electrophysiologically identified arm representations in the mesial agranular frontal cortex. Experimental Brain Research 82, 214218CrossRefGoogle ScholarPubMed
Luppino, G., Matelli, M., Camarda, R.M., Gallese, V. & Rizzolatti, G. (1991). Multiple representations of body movements in mesial area 6 and the adjacent cingulate cortex: An intracortical microstimulation study in the macaque monkey. Journal of Comparative Neurology 311, 463482CrossRefGoogle ScholarPubMed
Mann, S.E., Thau, R. & Schiller, P.H. (1988). Conditional task-related responses in monkey dorsomedial frontal cortex. Experimental Brain Research 69, 460468CrossRefGoogle ScholarPubMed
Matelli, M., Luppino, G. & Rizzolatti, G. (1991). Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. Journal of Comparative Neurology 311, 445462CrossRefGoogle ScholarPubMed
Mitz, A.R. & Godschalk, M. (1989). Eye movement representation in the frontal lobe of rhesus monkeys. Neuroscience Letters 106, 157162CrossRefGoogle ScholarPubMed
Mitz, A.R. & Wise, S.P. (1987). The somatotopic organization of the supplementary motor area: Intracortical microstimulation mapping. Journal of Neuroscience 7, 10101021CrossRefGoogle ScholarPubMed
Mushiake, H., Inase, M. & Tanji, J. (1991). Neuronal activity in the primate premotor, supplementary, and precentral motor cortex during visually guided and internally determined sequential movements. Journal of Neurophysiology 66, 705718CrossRefGoogle ScholarPubMed
Preuss, T.M. & Goldman-Rakic, P.S. (1991). Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions of the strepsirhine primate Galago and the anthropoid primate Macaca. Journal of Comparative Neurology 310, 429474CrossRefGoogle ScholarPubMed
Robinson, D.A. & Fuchs, A.F. (1969). Eye movements evoked by stimulation of frontal eye fields. Journal of Neurophysiotogy 32, 637648CrossRefGoogle ScholarPubMed
Russo, G.S. & Bruce, C.J. (1990). Quantitative analysis of the trajectory of electrically elicited saccadic eye movements in the frontal eye field and supplementary eye field of the monkey. Society for Neuroscience Abstracts 16, 899.Google Scholar
Russo, G.S. & Bruce, C.J. (1991). Response fields of neurons in the supplementary eye field of the rhesus monkey are retinotopic. Society for Neuroscience Abstracts 17, 462.Google Scholar
Schall, J.D. (1991 a). Neural basis of saccadic eye movements in primates. In Vision and Visual Dysfunction. Vol. 4: The Neural Basis of Visual Function, ed. Leventhal, A.G., pp. 388442. London: MacMillan Press.Google Scholar
Schall, J.D. (1991 b). Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of rhesus monkeys. Journal of Neurophysiology 66, 530558CrossRefGoogle ScholarPubMed
Schall, J.D. (1991 c). Neuronal activity related to visually guided saccades in the frontal eye fields of rhesus monkeys: Comparison with supplementary eye fields. Journal of Neurophysiotogy 66, 559579CrossRefGoogle ScholarPubMed
Schall, J.D., Mann, S.E. & Schiller, P.H. (1987). Investigation of the roles of dorsomedial and ventrolateral premotor regions and the frontal eye fields in visually guided movements. Society for Neuroscience Abstracts 13, 1095.Google Scholar
Schall, J.D., Morel, A., King, D.J., Bullier, J. & Kaas, J.H. (1992). Topographic organization of cortical visual afferents to frontal eye field in macaque: Functional convergence and segregation of processing streams (in preparation).Google Scholar
Schiller, P.H., True, S.D. & Conway, J.L. (1980). Deficits in eye movements following frontal eye field and superior colliculus ablations. Journal of Neurophysiology 44, 11751189CrossRefGoogle ScholarPubMed
Schiller, P.H., Sandell, J.H. & Maunsell, J.H.R. (1987). The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. Journal of Neurophysiology 57, 10331049CrossRefGoogle ScholarPubMed
Schlag, J. & Schlag-Rey, M. (1985). Eye fixation units in the supplementary eye field of monkey. Society for Neuroscience Abstracts 11, 82.Google Scholar
Schlag, J. & Schlag-Rey, M. (1986). Role of central thalamus and supplementary eye field in voluntary control of gaze in space. Bulletin of Tokyo Metropolitan Institute for Neurosciences (Suppl.) 1731Google Scholar
Schlag, J. & Schlag-Rey, M. (1987). Evidence for a supplementary eye field. Journal of Neurophysiology 57, 179200CrossRefGoogle ScholarPubMed
Segraves, M.A. & Goldberg, M.E. (1987). Functional properties of corticotectal neurons in the monkey’s frontal eye fields. Journal of Neurophysiology 58, 13871419CrossRefGoogle Scholar
Shook, B.L., Schlag-Rey, M. & Schlag, J. (1990). Primate supplementary eye field: I. Comparative aspects of mesencephalic and pontine connections. Journal of Comparative Neurology 301, 618642CrossRefGoogle ScholarPubMed
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, 4563CrossRefGoogle ScholarPubMed
Stanton, G.B. (1986). Frontal eye-field (FEF) connections with dorsomedial area 6 in the macaque monkey. Society for Neuroscience Abstracts 12, 455.Google Scholar
Stanton, G.B., Deng, S.-Y., Goldberg, M.E. & McMullen, N.T. (1989). Cytoarchitectural characteristics of the frontal eye fields in macaque monkeys. Journal of Comparative Neurology 282, 415427CrossRefGoogle ScholarPubMed
Tehovnik, E.J. & Lee, K.M. (1990). Electrical stimulation of the dorsomedial frontal cortex (DMFC) of the rhesus monkey. Society for Neuroscience Abstracts 16, 900.Google Scholar
Tehovnik, E.J., Lee, K.M. & Schiller, P.H. (1991). Effect of frontal eye field or superior colliculus lesions on stimulation-evoked saccades elicited from the primate dorsomedial frontal cortex. Society for Neuroscience Abstracts 17, 458.Google Scholar
Van Essen, D.C. & Maunsell, J.H.R. (1980). Two-dimensional maps of the cerebral cortex. Journal of Comparative Neurology 191, 255281CrossRefGoogle ScholarPubMed
Walker, A.E. (1940). A cytoarchitectural study of the prefrontal area of the macaque monkey. Journal of Comparative Neurology 73, 5986CrossRefGoogle Scholar
Yarbus, A.L. (1967). Eye Movements and Vision. New York: Plenum Press.CrossRefGoogle Scholar
Zipser, D. & Andersen, R.A. (1988). A back-propagation programmed network that simulates response properties of a subset of posterior parietal neurons. Nature 331, 679684CrossRefGoogle ScholarPubMed