Abstract
Smooth pursuit eye movements were studied in monkeys tracking target spots that moved two-dimensionally. Complex target trajectories were created by applying either two or three sinusoids to horizontal and vertical axes in various combinations. The chance of observing predictable performance was increased by repeated training on each trajectory. Data analyses were based upon repeated presentations of each trajectory within sessions and on successive days. We wished to determine how accurately monkeys could pursue targets moving along these trajectories and to observe interactions among frequency components. At intermediate frequencies, tracking performance was smooth and consistent during repeated presentations with saccadic corrections that were well integrated with smooth pursuit. The mean gain for eight different sum-of-sines trajectories was 0.83 and the mean magnitude (absolute value) of the phase error was 6°. In light of the long delays that have been associated with the processing of visual information, these values indicate that the monkeys were pursuing predictively. Five factors influenced predictive pursuit performance: (1) there was a decline in performance with increasing frequency; (2) horizontal pursuit was better than vertical pursuit; (3) high-frequency components were tracked with higher gains and phase lags, while lower-frequency components were tracked with lower gains and phase leads; (4) the gain of sinusoidal pursuit was always reduced when a second sinusoid was applied to the same axis or, to a lessor extent, when a second sinusoid of higher frequency was applied to the orthogonal axis; (5) the phase of sinusoidal pursuit shifted from a phase lag to a phase lead when combined with a second sinusoid of higher frequency, but was not affected by the addition of a lower-frequency sinusoid. Findings 1 and 2 confirm, in monkeys, results reported for humans, and 3 extends to monkeys and to two-dimensional pursuit results based upon human subjects. All of these findings demonstrate that complex predictive tracking is controlled by a nonlinear and nonhomogeneous system that uses predictive strategies in concert with feedback control to generate good pursuit.
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References
Bahill AT, McDonald JD (1983) Smooth pursuit eye movements in response to predictable target motions. Vision Res 23:1573–1583
Balaban CD, Watanabe E (1984) Functional representation of eye movements in the flocculus of monkeys (Macaca fuscata). Neurosci Lett 49:199–205
Balaban CD, Ito M, Watanabe E (1981) Demonstration of zonal projections from the cerebellar flocculus to vestibular nuclei in monkeys (Macaca fuscata). Neburosci Lett 27:101–105
Baloh RW, Yee RD, Honrubia V, Jacobson K (1988) A comparison of the dynamics of horizontal and vertical smooth pursuit in normal human subjects Aviat Space Environ Med 59:121–124
Barnes GR, Ruddock CJS (1989) Factors affecting the predictability of pseudo-random motion stimuli in the pursuit reflex of man. J Physiol (Lond) 408:137–165
Barnes GR, Donnelly SF, Eason RD (1987) Predictive velocity estimation in the pursuit reflex response to pseudo-random and step displacement stimuli in man. J Physiol (Lond) 389:111–136
Becker W, Fuchs AF (1984) Prediction in the oculomotor system: smooth pursuit during transient disappearance of a visual target. Exp Brain Res 57:562–575
Belknap DB, Noda H (1987) Eye movements evoked by microstimulation in the flocculus of the alert macaque. Exp Brain Res 67:352–362
Chubb MC, Fuchs AF (1982) Contribution of y group of vestibular nuclei and dentate nucleus of cerebellum to generation of vertical smooth eye movements. J Neurophysiol 48:75–99
Chubb MC, Fuchs AF, Scudder CA (1984) Neuron activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52:724–742
Collewijn H, Tamminga EP (1984) Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol (Lond) 351:217–250
Collewijn H, Van der Mark F, Jansen TC (1975) Precise recording of human eye movements. Vision Res 15:447–450.
Dallos PJ, Jones RW (1963) Learning behavior of the eye fixation control system. IEEE Trans Automat Control 8:218–227
Fuchs AF (1967) Saccadic and smooth pursuit eye movements in the monkey. J Physiol (Lond) 191:609–631
Fuchs AF, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161
Fukashima K, Perlmutter SI, Baker JF, Peterson BW (1990) Spatial properties of second-order vestibulo-ocular relay neurons in the alert cat. Exp Brain Res 81:462–478
Graf W, Baker J, Peterson BW (1993) Sensorimotor transformation in the cat's vestibuloocular reflex system. I. Neuronal signals coding spatial coordination of compensatory eye movements. J Neurophysiol 70:2425–2441
Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20:535–538
Kawano K, Shidara M, Yamane S (1992) Neuronal activity in dorsolateral pontine nucleus of alert monkey during ocular following responses. J Neurophysiol 67:680–703
Kawano K, Shidara M, Watanabe Y, Yamane S (1994) Neuronal activity in cortical area MST of alert monkey during ocularfollowing responses. J Neurophysiol 71:2305–2324
Kettner RE, Leung H-C, Giswold ME, Peterson BW (1994) Two dimensional smooth pursuit eye movements during tracking of double sine waves in monkey. Soc Neurosci Abstr 20:1193
Kowler E, Steinman RM (1979) The effect of expectations on slow oculomotor control. I. Periodic target steps. Vision Res 19:619–632
Krauzlis RJ, Lisberger SG (1989) A control systems model of smooth pursuit eye movements with realistic emergent properties. Neural Comp 1:116–122
Langer T, Kaneko CRS, Scudder CA, Fuchs AF (1986) Afferents to the abducens nucleus in the monkey and cat. J Comp Neurol 245:379–400
Leung H-C, Kettner RE (1995) Predictive control of smooth pursuit eye movements along complex two-dimensional trajectories in monkey. Soc Neurosci Abstr 21:140
Leung H-C, Kettner RE, Giswold ME, Peterson BW (1994) Two dimensional smooth pursuit eye movements during circular tracking and perturbations in monkey. Soc Neurosci Abstr 20:1193
Lisberger SG, Fuchs AF (1978a) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smoothpursuit eye movements and passive head rotation. J Neurophysiol 41:733–763
Lisberger SG, Fuchs AF (1978b) Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement. J Neurophysiol 41:764–777
Lisberger SG, Evinger C, Johanson GW, Fuchs AF (1981) Relationship between acceleration and retinal image velocity during foveal smooth pursuit in man and monkey. J Neurophysiol 46:229–249
Maunsel JHR, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49:1127–1147
McCrea RA, Strassman A, May E, Highstein SM (1987a) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex in the squirrel monkey. J Comp Neurol 264:547–570
McCrea RA, Strassman A, Highstein SM (1987b) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflex in the squirrel monkey. J Comp Neurol 264:571–594
McFarland JL, Fuchs AF (1992) Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J Neurophysiol 68:319–332.
Miles FA, Fuller JH, Braitman DJ, Dow BM (1980) Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol 43:1437–1476
Mustari MJ, Fuchs AF (1989) Response properties of single units in the lateral terminal nucleus of the accessory optic system in the behaving primate. J Neurophysiol 61:1207–1220
Mustari MJ, Fuchs AF, Wallman J (1988) Response properties of dorsolateral pontine units during smooth pursuit in the rhesus macaque. J Neurophysiol 60:664–686.
Pola J, Wyatt H (1980) Target position and velocity: the stimuli for smooth pursuit eye movements. Vision Res 20:523–534
Powell KD, Quinn KJ, Barke LD, Peterson BW (1992) Spatial properties of flocculus neurons in the decerebrate cat. Soc Neurosci Abstr 18:406
Powell KD, Killian JE, Peterson BW (1994) Maximum activation direction and visual-vestibular interaction of flocculus purkinje cells in alert cats. Soc Neurosci Abstr 20:1746
Press WH, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical recipes in C: The art of scientific computing, 2nd edn. Cambridge University Press, Cambridge
Rashbass C (1961) The relationship between saccadic and smooth tracking eye movements. J Physiol (Lond) 159:326–338
Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Electron 10:137–145
Robinson DA (1965) The mechanics of human smooth pursuit eye movements. J Physiol (Lond) 180:569–591
Robinson DA, Gordon JL, Gordon SE (1986) A model of the smooth pursuit eye movement system. Biol Cybern 55:43–57
Sato Y, Kawasaki T (1991) Identification of the purkinje cell/climbing fiber zone and its target neurons responsible for eye-movement control by the cerebellar flocculus. Brain Res Brain Res Rev 16:39–64
Sato Y, Kawasaki T, Ikarashi (1983) Afferent projections from the brainstem to the three floccular zones in cats. II. mossy fiber projections. Brain Res 272:37–48
Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J. Neurophysiol 68:244–264.
Stone LS, Lisberger SG (1990a) Visual responses of purkinje cells in the cerebellar flocculus during smooth pursuit eye movements in monkeys I. Simple spikes. J Neurophysiol 63(5):1241–1261
Stone LS, Lisberger SG (1990b) Visual responses of purkinje cells in the cerebellar flocculus during smooth pursuit eye movements in monkeys II. Complex spikes. J Neurophysiol 63:1262–1275
Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51:1121–1136.
Van den Berg AV (1988) Human smooth pursuit during transient perturbations of predictable and unpredictable target movement. Exp Brain Res 72:95–108
Winer BJ, Brown DR, Michels KM (1991) Statistical principles in experimental design, 3rd edn. McGraw-Hill, New York
Yasui S, Young LR (1984) On the predictive control of foveal eye tracking and slow phases of optokinetic and vestibular nystagmus. J Physiol (Lond) 347:17–33
Zee DS, Atsumi Y, Butler PH, Güçer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primate. J Neurophysiol 46:878–899
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Kettner, R.E., Leung, HC. & Peterson, B.W. Predictive smooth pursuit of complex two-dimensional trajectories in monkey: component interactions. Exp Brain Res 108, 221–235 (1996). https://doi.org/10.1007/BF00228096
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DOI: https://doi.org/10.1007/BF00228096