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Single-neuron activity in the dorsomedial frontal cortex during smooth-pursuit eye movements to predictable target motion

Published online by Cambridge University Press:  02 June 2009

S. J. Heinen  and
M. Liu
S. J. Heinen
Affiliation:
The Smith-Kettlewell Eye Research Institute, San Francisco
M. Liu
Affiliation:
The Smith-Kettlewell Eye Research Institute, San Francisco
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Abstract

A region of dorsomedial frontal cortex (DMFC) has been implicated in planning and executing saccadic eye movements; hence it has been referred to as a supplementary eye field (SEF). Recently, activity related to executing smooth-pursuit eye movements has been recorded from the DMFC, and microstimulation here has been shown to evoke smooth eye movements. This report documents neuronal activity present in smooth-pursuit tasks where the predictability of target motion was manipulated. The activity of many neurons in the DMFC reached a peak when a predictable change in target motion occurred. Furthermore, the peak activity of some cells was systematically shifted by manipulating the duration of the target event, indicating that the network these neurons were in could learn the temporal characteristics of new target motion. Finally, the activity of most neurons tested was greater when target motion was predictable than when it was unpredictable. The results suggest that the DMFC participates in planning smooth-pursuit eye movements based on past stimulus history.

Keywords

MonkeyPremotorSEFEye movements
Type
Research Articles
Information
Visual Neuroscience , Volume 14 , Issue 5 , September 1997 , pp. 853 - 865
Copyright
Copyright © Cambridge University Press 1997

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References

Barbas, H. & Mesulam, M.M. (1985). Cortical afferent input to the principalis region of the rhesus monkey. Neuroscience 15, 619–637.CrossRefGoogle Scholar
Barnes, G.R. & Ruddock, C.J.S. (1972). Factors affecting the predictability of pseudo-random motion stimuli in the pursuit reflex of man. Journal of Physiology (London) 408, 137–165.CrossRefGoogle Scholar
Becker, W., Hoehne, O., Iwase, K. & Kornhuber, H.H. (1972). Bereit-shaftpotential, pramotorische positivierung und andere Hirnpotentiale bei sakkadischen Augenbewegungen. Vision Research 12, 421–436.CrossRefGoogle Scholar
Boman, D.K. & Hotson, J.R. (1992). Predictive smooth pursuit eye movements near abrupt changes in motion direction. Vision Research 32, 675–689.CrossRefGoogle ScholarPubMed
Brodmann, K. (1909). Vergleichende Lokalisationslehre der Groshirn-rinde. Leipzig: Barth (reprinted 1925).$$$Google Scholar
Dallos, P.J. & Jones, R.W. (1963). Learning behavior of the eye fixation control system. IEEE Transactions on Automatic Control AC-8, 218–227.CrossRefGoogle Scholar
Deeke, L. & Kornhuber, H.H. (1977). Cerebral potentials and the initiation of voluntary movement. In Progress in Clinical Neurophysiology, ed. Desmedt, J.E., Vol. 1, pp. 132–150. Basel: Karger.Google Scholar
Deno, D.C., Crandall, W.F., Sherman, K. & Keller, E.L. (1994). Characterization of prediction in the primate visual smooth pursuit system. Biosystems 34, 107–128.CrossRefGoogle Scholar
Dodge, R., Travis, R.C. & Fox, J.C. (1930). Optic nystagmus III. Characteristics of the slow phase. Archives of Neurological Psychiatry 24, 21–34.CrossRefGoogle Scholar
Evdokimidis, I., Mergner, T. & Lucking, C.H. (1992). Dependence of presaccadic cortical potentials on the type of saccadic eye movement. Electroencephalography and Clinical Neurophysiology 83, 179–191.CrossRefGoogle ScholarPubMed
Fuchs, A.F. (1967). Periodic eye tracking in the monkey. Journal of Physiology (London) 193, 161–171.CrossRefGoogle ScholarPubMed
Gaymard, B., Pierrot-Deseilligny, C. & Rivaud, S. (1990). Impairment of sequences of memory-guided saccades after supplementary motor area lesions. Annals of Neurology 28, 622–626.CrossRefGoogle ScholarPubMed
Goldberg, G. (1985). Supplementary motor area structure and function: Review and hypotheses. The Behavioral and Brain Sciences 8, 567–616.Google Scholar
Goldreich, D., Krauzlis, R.J. & Lisberger, S.G. (1992). Effect of changing feedback delay on spontaneous oscillations in smooth pursuit eye movements of monkeys. Journal of Neurophysiology 67, 625–638.CrossRefGoogle ScholarPubMed
Grasse, K.L. & Lisberger, S.G. (1992). Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey. Journal of Neurophysiology 67, 164–179.Google Scholar
Heinen, S.J. (1995 a). Single-neuron activity in dorsomedial frontal cortex during smooth pursuit eye movements. Experimental Brain Research 104, 357–361.CrossRefGoogle ScholarPubMed
Heinen, S.J. (1995 b). A model of predictive smooth pursuit based on timing of target motion. Society for Neuroscience Abstracts 21, 520.Google Scholar
Huerta, M.F & Kaas, J.H. (1990). Supplementary eye field as defined by intracortical micro-stimulation: Connections in macaques. Journal of Comparative Neurology 293, 299–330.CrossRefGoogle Scholar
Huerta, M.F., Krubitzer, L.A. & Kaas, J.H. (1987). Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys: II. Cortical connections. Journal of Comparative Neurology 265, 332–361.CrossRefGoogle ScholarPubMed
Judge, S.J., Richmond, B.J. & Chu, F.C. (1980). Implantation of magnetic search coils for measurement of eye position: An improved method. Vision Research 20, 535–538.CrossRefGoogle ScholarPubMed
Kao, G.W. & Morrow, M.J. (1994). The relationship of anticipatory smooth eye movement to smooth pursuit initiation. Vision Research 34, 3027–3036.CrossRefGoogle ScholarPubMed
Keller, E.L. & Kahn, N.S. (1986). Smooth-pursuit initiation in the presence of a textured background in monkey. Journal of Neurophysiology 68, 2147–2164.Google Scholar
Kowler, E. & Steinman, R.M. (1979). The effect of expectations on slow oculomotor control—I. Periodic target steps. Vision Research 19, 619–632.Google Scholar
Kowler, E. (1990). The role of visual and cognitive processes in the control of eye movement. In Eye Movements and Their Role in Visual and Cognitive Processes, ed. Kowler, E., pp. 1–70. Amsterdam, Holland: Elsevier.Google ScholarPubMed
Kowler, E., Steinman, R., He, P. & Pizlo, Z. (1989). Smooth pursuit depends on the expected duration of target motion. Investigative Ophthalmology and Visual Science (Suppl.) 30, 182.Google Scholar
Krauzlis, R.J. & Lisberger, S.G. (1994). Temporal properties of visual motion signals for the initiation of smooth pursuit eye movements in monkeys. Journal of Neurophysiology 72, 150–162.CrossRefGoogle ScholarPubMed
Lee, K. & Tehovnik, E.J. (1995). Topographic distribution of fixation-related units in the dorsomedial frontal cortex of the rhesus monkey. European Journal of Neuroscience 7, 1005–1011.CrossRefGoogle ScholarPubMed
Libet, B., Wright, E.W. Jr & Gleason, C.A. (1982 a). Preparation-or intention-to-act in relation to pre-event potentials recorded at the vertex. Electroencephalography and Clinical Neurophysiology 56, 367–372.CrossRefGoogle Scholar
Libet, B., Wright, E.W. Jr & Gleason, C.A. (1982 b). Readiness-potentials preceding unrestricted “spontaneous” vs. preplanned voluntary acts. Electroencephalography and Clinical Neurophysiology 54, 322–335.Google Scholar
Mann, S., Thau, R. & Schiller, P.H. (1988). Conditional task-related responses in monkey dorsomedial frontal cortex. Experimental Brain Research 69, 460–468.CrossRefGoogle ScholarPubMed
Newsome, W.T., Wurtz, R.H. & Komatsu, H. (1988). Relation of cortical MT and MST to pursuit eye movements II. Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology 60, 604–620.Google Scholar
Petit, L., Orssaud, C., Tzourio, N., Salamon, G., Mazoyer, B. & Berthoz, A. (1993). PET study of voluntary saccadic eye movements in humans: Basal ganglia-thalamocortical system and cingulate cortex involvement. Journal of Neurophysiology 69, 1009–1017.Google Scholar
Rashbass, C. (1961). The relationship between saccadic and smooth tracking eye movements. Journal of Physiology (London) 159, 326–338.CrossRefGoogle ScholarPubMed
Richmond, B.J., Optican, L.M., Podell, M. & Spitzer, H. (1987). Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. Journal of Neurophysiology 57, 132–146.CrossRefGoogle ScholarPubMed
Robinson, D.A. (1963). A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Transactions on Bio-Medical Engineering BME-10, 137–145.Google ScholarPubMed
Robinson, D.A. (1981). Control of eye movements. In Handbook of Physiology, Vol. II, Part 2, The Nervous System, ed. Brooks, V.B., pp. 1275–1320. Bethesda, Maryland: American Physiology Society.Google Scholar
Roland, P.E., Larsen, B., Lassen, N.A. & Skinhof, E. (1980). Supplementary motor area and other cortical areas in organization of voluntary movements in man. Journal of Neurophysiology 43, 118–136.Google Scholar
Schall, J.D. (1991). Neuronal activity related to visually guided saccadic eye movements in the supplementary motor area of Rhesus monkeys. Journal of Neurophysiology 66, 530–558.Google Scholar
Schlag, J. & Schlag-Rey, M. (1987). Evidence for a supplementary eye field. Journal of Neurophysiology 57, 179–200.CrossRefGoogle ScholarPubMed
Schlag, J., Schlag-Rey, M. & Pigarev, I. (1992). Supplementary eye field: Influence of eye position on neural signals of fixation. Experimental Brain Research 90, 302–306.CrossRefGoogle ScholarPubMed
Stark, L., Vossius, G. & Young, L.R. (1962). Predictive control of eye tracking movements. IRE Transactions on Human Factors in Electronics 3, 52–57.Google Scholar
Suzuki, D.A., Yamada, T., Betelak, K.F. & Yee, R.D. (1991). Smooth-pursuit eye movement related activity in monkey nucleus reticularis tegmenti pontis. Society of Neuroscience Abstracts 17, 459.Google Scholar
Tanji, J. & Shima, K. (1994). Role for supplementary motor area cells in planning several movements ahead. Nature 371, 413–416.CrossRefGoogle ScholarPubMed
Tehovnik, E.J. & Lee, K. (1993). The dorsomedial frontal cortex of the rhesus monkey: Topographic representation of saccades evoked by electrical stimulation. Experimental Brain Research 96, 430–442.CrossRefGoogle ScholarPubMed
Tian, J. & Lynch, J.C. (1995). Slow and saccadic eye movements evoked by microstimulation in the supplementary eye field of the cebus monkey. Journal of Neurophysiology 74, 2204–2210.Google Scholar
Westheimer, G. (1954). Eye movement responses to a horizontally moving visual stimulus. A.M.A. Archives of Ophthalmology 52, 932–941.CrossRefGoogle ScholarPubMed
Wise, S.P. & Tanji, J. (1981). Supplementary and precentral motor cortex: Contrast in responsiveness to peripheral input in the hindlimb area of the unanesthetized monkey. Journal of Comparative Neurology 195, 433–451.CrossRefGoogle ScholarPubMed