Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity.

Saccade accuracy is known to be maintained by adaptive mechanisms that progressively reduce any visual error that consistently exists at the end of saccades. Experimentally, the visual error is induced using one of two paradigms. In the first, the horizontal and medial recti of trained monkeys are tenectomized and allowed to reattach so that both muscles are paretic. After patching the unoperated eye and forcing the monkey to use the "paretic eye," saccades initially undershoot the intended target, but gradually increase in size until they almost acquire the target in one step. In the second, the target of a saccade is displaced in midsaccade so that the saccade cannot land on target. Again saccade size adapts until the target can be acquired in one step. Because adaptation with the latter paradigm is very rapid but adaptation using the former is slow, it has frequently been questioned whether or not the two forms of adaptation depend on the same neural mechanisms. We show that the rate of adaptation in both paradigms depends on the number of possible visual targets, so that when this variable is equated, adaptation occurs at similar rates in both paradigms. To demonstrate further similarities between the result of the two paradigms, an experiment using intrasaccadic displacements was conducted to show that rapid adaptation possesses the capacity to produce gain changes that vary with orbital position. The relative size of intrasaccadic displacements were graded with orbital position so as to mimic the position-dependent dysmetria initially produced by a single paretic extraocular muscle. Induced changes in saccade size paralleled the size of the displacements, being largest for saccades into one hemifield and being negligible for saccades into the other hemifield or in the opposite direction. Collectively, the data remove the rational for asserting that adaptation produced by the two paradigms depends on separate neural mechanisms. We argue that adaptation produced by both paradigms depends on the cerebellum.

[1]  S. C. Mclaughlin Parametric adjustment in saccadic eye movements , 1967 .

[2]  Glenn E. Weisfeld,et al.  Parametric adjustment to a shifting target alternating with saccades to a stationary reference point , 1972 .

[3]  G. Kommerell,et al.  Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. , 1976, Investigative ophthalmology.

[4]  D. Robinson Adaptive gain control of vestibuloocular reflex by the cerebellum. , 1976, Journal of neurophysiology.

[5]  D. Henson Corrective saccades: Effects of altering visual feedback , 1978, Vision Research.

[6]  L. Dell’Osso,et al.  Saccadic system plasticity in humans , 1978, Annals of neurology.

[7]  B. Richmond,et al.  Implantation of magnetic search coils for measurement of eye position: An improved method , 1980, Vision Research.

[8]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

[9]  H. Noda,et al.  Discharges of Purkinje cells and mossy fibres in the cerebellar vermis of the monkey during saccadic eye movements and fixation , 1980, The Journal of physiology.

[10]  J. E. Albano,et al.  Visual-motor function of the primate superior colliculus. , 1980, Annual review of neuroscience.

[11]  F A Miles,et al.  Long-term adaptive changes in primate vestibuloocular reflex. I. Behavioral observations. , 1980, Journal of neurophysiology.

[12]  D. Zee,et al.  Effects of ablation of flocculus and paraflocculus of eye movements in primate. , 1981, Journal of neurophysiology.

[13]  W. B. Templeton,et al.  Saccadic plasticity: parametric adaptive control by retinal feedback. , 1981, Journal of experimental psychology. Human perception and performance.

[14]  F A Miles,et al.  Signals used to compute errors in monkey vestibuloocular reflex: possible role of flocculus. , 1984, Journal of neurophysiology.

[15]  W. Wolf,et al.  Properties of Parametric Adjustment in the Saccadic System , 1984 .

[16]  Optican Lm Adaptive properties of the saccadic system. , 1985 .

[17]  T Vilis,et al.  Adaptation of saccadic and vestibulo-ocular systems after extraocular muscle tenectomy. , 1985, Investigative ophthalmology & visual science.

[18]  E. Keller,et al.  Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. , 1985, Journal of neurophysiology.

[19]  A. Fuchs,et al.  Brainstem control of saccadic eye movements. , 1985, Annual review of neuroscience.

[20]  L. Optican,et al.  Adaptive response to ocular muscle weakness in human pursuit and saccadic eye movements. , 1985, Journal of neurophysiology.

[21]  L M Optican,et al.  Adaptive properties of the saccadic system. , 1985, Reviews of oculomotor research.

[22]  Adaptive modulation of VOR parameters by vision. , 1985, Reviews of oculomotor research.

[23]  Jones Gm Adaptive modulation of VOR parameters by vision. , 1985 .

[24]  H Deubel,et al.  Adaptive gain control of saccadic eye movements. , 1986, Human neurobiology.

[25]  H. Deubel ADAPTIVITY OF GAIN AND DIRECTION IN OBLIQUE SACCADES1 , 1987 .

[26]  A. Fuchs,et al.  Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. , 1988, Journal of neurophysiology.

[27]  W. Becker The neurobiology of saccadic eye movements. Metrics. , 1989, Reviews of oculomotor research.

[28]  D. Sparks,et al.  The deep layers of the superior colliculus. , 1989, Reviews of oculomotor research.

[29]  J. Vercher,et al.  Mechanisms of short-term saccadic adaptation. , 1989, Journal of experimental psychology. Human perception and performance.

[30]  M. Ito,et al.  Long-term depression. , 1989, Annual review of neuroscience.

[31]  J E Albano,et al.  Rapid adaptation of saccadic amplitude in humans and monkeys. , 1989, Investigative ophthalmology & visual science.

[32]  H. Noda,et al.  Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey , 1990, The Journal of comparative neurology.

[33]  F. Crépel,et al.  Pairing of pre‐ and postsynaptic activities in cerebellar Purkinje cells induces long‐term changes in synaptic efficacy in vitro. , 1991, The Journal of physiology.

[34]  A. Marty,et al.  Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents , 1991, Neuron.

[35]  M. Dickinson,et al.  A long-term depression of AMPA currents in cultured cerebellar purkinje neurons , 1991, Neuron.

[36]  The Error Signal for Modification of Vestibuloocular Reflex Gain , 1992, Annals of the New York Academy of Sciences.

[37]  R. Abrams,et al.  Adaptive modification of saccadic eye movements. , 1992 .

[38]  K. Ohtsuka,et al.  Burst discharges of mossy fibers in the oculomotor vermis of macaque monkeys during saccadic eye movements , 1992, Neuroscience Research.

[39]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. , 1994, Journal of neurophysiology.

[40]  S. Lisberger,et al.  Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons. , 1994, Journal of neurophysiology.

[41]  Heiner Deubel,et al.  Rapid gain adaptation affects the dynamics of saccadic eye movements in humans , 1995, Vision Research.

[42]  J. V. Van Gisbergen,et al.  Short-term adaptation of electrically induced saccades in monkey superior colliculus. , 1996, Journal of neurophysiology.

[43]  J. E. Albano Adaptive Changes in Saccade Amplitude: Oculocentric or Orbitocentric Mapping? , 1996, Vision Research.

[44]  A. Fuchs,et al.  Transfer of gain changes from targeting to other types of saccade in the monkey: constraints on possible sites of saccadic gain adaptation. , 1996, Journal of neurophysiology.

[45]  A. Opstal,et al.  Monkey Superior Colliculus Activity During Short-Term Saccadic Adaptation , 1997, Brain Research Bulletin.

[46]  A. Fuchs,et al.  Characteristics of saccadic gain adaptation in rhesus macaques. , 1997, Journal of neurophysiology.