Abstract
The primate superior colliculus (SC) is a midbrain nucleus crucial for the control of rapid eye movements (saccades). Its neurons are topographically arranged over the rostrocaudal and mediolateral extent of its deeper layers so that saccade metrics (amplitude and direction) are coded in terms of the location of active neurons. We used the quantitative [14C]-deoxyglucose method to obtain a map of the two-dimensional pattern of activity throughout the SC of rhesus monkeys repeatedly executing visually guided saccades of the same amplitude and direction for the duration of the experiment. Increased metabolic activity was confined to a circumscribed region of the two-dimensional reconstructed map of the SC contralateral to the direction of the movement. The precise rostrocaudal and mediolateral location of the area activated depended on saccade metrics. Our data support the notion that the population of active SC cells remains stationary in collicular space during saccades.
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References
Moschovakis, A. K. The superior colliculus and eye movement control. Curr. Opin. Neurobiol. 6, 811–816 (1996).
Kadoya, S., Wolin, L. R. & Massopust, L. C. J. Photically evoked unit activity in the tectum opticum of the squirrel monkey. J. Comp. Neurol. 142, 495–508 (1971).
Cynader, M. & Berman, N. Receptive-field organization of monkey superior colliculus. J. Neurophysiol. 35, 187–201 (1972).
Updike, B. V. Characteristics of unit responses in superior colliculus of the Cebus monkey. J. Neurophysiol. 37, 896–909 (1974).
Schiller, P. H. & Stryker, M. Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35, 915–924 (1972).
Wurtz, R. E. & Goldberg, M. E. Activity of superior colliculus in behaving monkey. III. Cells discharging before eye movements. J. Neurophysiol. 35, 575–586 (1972).
Sparks, D. L. Functional properties of neurons in the monkey superior colliculus: coupling of neuronal activity and saccade onset. Brain Res. 156, 1–16 (1978).
Droulez, J. & Berthoz, A. A neural network model of sensoritopic maps with predictive short-term memory properties. Proc. Natl. Acad. Sci. USA 88, 9653–9657 (1991).
Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey superior colliculus. II. Spread of activity during saccades. J. Neurophysiol. 73, 2334–2348 (1995).
Optican, L. M. A field theory of saccade generation: temporal-to-spatial transform in the superior colliculus. Vision Res. 35, 3313–3320 (1995).
Waitzman, D. M., Ma, T. P., Optican, L. M. & Wurtz, R. H. Superior colliculus neurons mediate the dynamic characteristics of saccades. J. Neurophysiol. 66, 1716–1737 (1991).
van Gisbergen, J. A. M., Robinson, D. A. & Gielen, S. A quantitative analysis of generation of sacccadic eye movements by burst neurons. J. Neurophysiol. 45, 417–442 (1981).
Scudder, C. A. A new local feedback model of the saccadic burst generator. J. Neurophysiol. 59, 1455–1475 (1988).
Moschovakis, A. K. Neural network simulations of the primate oculomotor system. I. The vertical saccadic burst generator. Biol. Cybern. 70, 291–302 (1994).
Bozis, A. & Moschovakis, A. K. Neural network simulations of the primate oculomotor system. III. A one-dimensional one-directional model of the superior colliculus. Biol. Cybern. 79, 215–230 (1998).
Ottes, F. P., van Gisbergen, J. A. M. & Eggermont, J. J. Visuomotor fields of the superior colliculus: a quantitative model. Vision Res. 26, 857–873 (1986).
Anderson, R. W., Keller, E. L., Gandhi, N. J. & Das, S. Two-dimensional saccade-related population activity in superior colliculus in monkey. J. Neurophysiol. 80, 798–817 (1998).
Sokoloff, L. et al. The [14C]deoxyglucose method for the measurment of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28, 897–916 (1977).
Sparks, D. L. & Mays, L. E. Movement fields of saccade-related burst neurons in the monkey superior colliculus. Brain Res. 190, 39–50 (1980).
Robinson, D. A. Eye movements evoked by collicular stimulation in the alert monkey. Vision Res. 12, 1795–1808 (1972).
van Opstal, A. J., van Gisbergen, J. A. M. & Smit, A. C. Comparison of saccades evoked by visual stimulation and collicular electrical stimulation in the alert monkey. Exp. Brain Res. 79, 299–312 (1990).
Goldberg, M. E. & Wurtz, R. H. Activity of superior colliculus in behaving monkey. II. Effect of attention on neuronal responses. J. Neurophysiol. 35, 560–574 (1972).
Munoz, D. P. & Wurtz, R. H. Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J. Neurophysiol. 70, 559–575 (1993).
Everling, S., Paré, M., Dorris, M. C. & Munoz, D. P. Comparison of the discharge characteristics of brain stem omnipause neurons and superior colliculus fixation neurons in monkey: implications for control of fixation and saccade behavior. J. Neurophysiol. 79, 511–528 (1998).
Krauzlis, R. J., Basso, M. A. & Wurtz, R. H. Discharge properties of neurons in the rostral superior colliculus in the monkey during smooth-pursuit eye movements. J. Neurophysiol. 84, 876–891 (2000).
Munoz, D. P., Pelisson, D. & Guitton, D. Movement of neural activity on the superior colliculus motor map during gaze shifts. Science 251, 1358–1360 (1991).
Munoz, D. P., Guitton, D. & Pelisson, D. Control of orienting gaze shifts by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal characteristics of phasic motor discharges. J. Neurophysiol. 66, 1642–1666 (1991).
Aizawa, H. & Wurtz, R. H. Reversible inactivation of monkey superior colliculus. I. Curvature of saccadic trajectory. J. Neurophysiol. 79, 2082–2096 (1998).
Sparks, D. L., Holland, R. & Guthrie, B. L. Size and distribution of movement fields in the monkey superior colliculus. Brain Res. 113, 21–34 (1976).
Moschovakis, A. K., Karabelas, A. B. & Highstein, S. M. Structure-function relationships in the primate superior colliculus. II. Morphological identity of presaccadic neurons. J. Neurophysiol. 60, 263–302 (1988).
Keller, E. L. & Edelman, J. A. Use of interrupted saccade paradigm to study spatial and temporal dynamics of saccade burst cells in superior colliculus in monkey. J. Neurophysiol. 72, 2754–2770 (1994).
Munoz, D. P., Waitzman, D. M. & Wurtz, R. H. Activity of neurons in monkey superior colliculus during interrupted saccades. J. Neurophysiol. 75, 2562–2580 (1996).
Port, N. L., Sommer, M. A. & Wurtz, R. H. Multielectrode evidence for spreading activity across the superior colliculus movement map. J. Neurophysiol. 84, 344–357 (2000).
Everling, S., Dorris, M. C., Klein, R. M. & Munoz, D. P. Role of primate superior colliculus in preparation and execution of anti-saccades and pro-saccades. J. Neurosci. 19, 2740–2754 (1999).
Munoz, D. P. & Wurtz, R. H. Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J. Neurophysiol. 73, 2313–2333 (1995).
Judge, S. J., Richmond, B. J. & Chu, F. C. Implantation of magnetic search coils for measurements of eye position: an improved method. Vision Res. 20, 535–538 (1980).
Robinson, D. A. A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans. Biomed. Engin. 10, 137–145 (1963).
Gregoriou, G. G. & Savaki, H. E. The intraparietal cortex: subregions involved in fixation, saccades and in the visual and somatosensory guidance of movement. J. Cereb. Blood Flow Metab. 21, 671–682 (2001).
Savaki, H. E., Kennedy, C., Sokoloff, L. & Mishkin, M. Visually guided reaching with the forelimb contralateral to a “blind” hemisphere: a metabolic mapping study in monkeys. J. Neurosci. 13, 2772–2789 (1993).
Dalezios, Y., Raos, V. C. & Savaki, H. E. Metabolic activity pattern in the motor and somatosensory cortex of monkeys performing a visually guided reaching task with one forelimb. Neuroscience 72, 325–333 (1996).
Savaki, H. E., Raos, V. C. & Dalezios, Y. Spatial cortical patterns of metabolic activity in monkeys performing a visually guided reaching task with one forelimb. Neuroscience 76, 1007–1034 (1997).
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The technical assistance of M. Koumaki and the financial support of BIO4-CT98-0546 are gratefully acknowledged.
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Moschovakis, A., Gregoriou, G. & Savaki, H. Functional imaging of the primate superior colliculus during saccades to visual targets. Nat Neurosci 4, 1026–1031 (2001). https://doi.org/10.1038/nn727
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DOI: https://doi.org/10.1038/nn727
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