Abstract
Motor learning ensures the accuracy of our daily movements. However, we know relatively little about its mechanisms, particularly for voluntary movements. Saccadic eye movements serve to bring the image of a visual target precisely onto the fovea. Their accuracy is maintained not by on-line sensory feedback but by a learning mechanism, called saccade adaptation. Recent studies on saccade adaptation have provided valuable additions to our knowledge of motor learning. This review summarizes what we know about the characteristics and neural mechanisms of saccade adaptation, emphasizing recent findings and new ideas. Long-term adaptation, distinct from its short-term counterpart, seems to be present in the saccadic system. Accumulating evidence indicates the involvement of the oculomotor cerebellar vermis as a learning site. The superior colliculus is now suggested not only to generate saccade commands but also to issue driving signals for motor learning. These and other significant contributions have advanced our understanding of saccade adaptation and motor learning in general.
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References
Abel LA, Schmidt D, Dell’Osso LF, Daroff RB (1978) Saccadic system plasticity in humans. Ann Neurol 4:313–318
Albano JE (1996) Adaptive changes in saccade amplitude: oculocentric or orbitocentric mapping? Vis Res 36:2087–2098
Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25–61
Bahcall DO, Kowler E (2000) The control of saccadic adaptation: implications for the scanning of natural visual scenes. Vis Res 40:2779–2796
Barash S, Melikyan A, Sivakov A, Zhang M, Glickstein M, Thier P (1999) Saccadic dysmetria and adaptation after lesions of the cerebellar cortex. J Neurosci 19:10931–10939
Becker W (1989) Metrics. In: Wurtz B, Goldberg M (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 13–67
Boyden ES, Raymond JL (2003) Active reversal of motor memories reveals rules governing memory encoding. Neuron 39:1031–1042
Brodal P (1980) The projection from the nucleus reticularis tegmenti pontis to the cerebellum in the rhesus monkey. Exp Brain Res 38:29–36
Carey MR, Medina JF, Lisberger SG (2005) Instructive signals for motor learning from visual cortical area MT. Nat Neurosci 8:813–819
Catz N, Dicke PW, Thier P (2005) Cerebellar complex spike firing is suitable to induce as well as to stabilize motor learning. Curr Biol 15:2179–2189
Catz N, Dicke PW, Thier P (2008) Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. Proc Natl Acad Sci U S A 105:7309–7914
Cecala AL, Freedman EG (2008) Amplitude changes in response to target displacements during human eye-head movements. Vis Res 48:149–166
Cecala AL, Freedman EG (2009) Head-unrestrained gaze adaptation in the rhesus macaque. J Neurophysiol 101:164–183
Chen-Harris H, Joiner WM, Ethier V, Zee DS, Shadmehr R (2008) Adaptive control of saccades via internal feedback. J Neurosci 28:2804–2813
Crandall WF, Keller EL (1985) Visual and oculomotor signals in nucleus reticularis tegmenti pontis in alert monkey. J Neurophysiol 54:1326–1345
Dean P, Mayhew JEW, Langdon P (1994) Learning and maintaining saccadic accuracy: a model of brainstem-cerebellar interactions. J Cogn Neurosci 6:117–138
Deubel H (1987) Adaptivity of gain and direction in oblique saccades. In: O’Regan J, Levy-Schoen A (eds) Eye movements: from physiology to cognition. Elsevier, Amsterdam, pp 181–191
Deubel H (1989) Sensory and motor aspects of saccade control. Eur Arch Psychiatry Neurol Sci 239:17–22
Deubel H (1991) Adaptive control of saccade metrics. In: Obrecht G, Stark L (eds) Presbyopia research. Plenum Press, New York, pp 93–100
Deubel H, Wolf W, Hauske G (1986) Adaptive gain control of saccadic eye movements. Hum Neurobiol 5:245–253
Ditterich J, Eggert T, Straube A (1999) Does visual background information influence saccadic adaptation? In: Becher W, Deubel H, Mergner T (eds) Current oculomotor research: physiological and psychological aspects. Plenum Press, New York, pp 71–80
Ditterich J, Eggert T, Straube A (2000) The role of the attention focus in the visual information processing underlying saccadic adaptation. Vis Res 40:1125–1134
Edelman JA, Goldberg ME (2002) Effect of short-term saccadic adaptation on saccades evoked by electrical stimulation in the primate superior colliculus. J Neurophysiol 87:1915–1923
Erkelens CJ, Hulleman J (1993) Selective adaptation of internally triggered saccades made to visual targets. Exp Brain Res 93:157–164
Ethier V, Zee DS, Shadmehr R (2008) Changes in control of saccades during gain adaptation. J Neurosci 28:13929–13937
Fitzgibbon E, Goldberg M, Segraves M (1986) Short term adaptation in the monkey. In: Keller EL, Zee DS (eds) Adaptive processes in visual and oculomotor systems. Pergamon Press, Oxford, pp 329–333
Frankfurter A, Weber JT, Royce GJ, Strominger NL, Harting JK (1976) An autoradiographic analysis of the tecto-olivary projection in primates. Brain Res 118:245–257
Frens MA, van Opstal AJ (1994) Transfer of short-term adaptation in human saccadic eye movements. Exp Brain Res 100:293–306
Frens M, van Opstal A (1997) Monkey superior colliculus activity during short-term saccadic adaptation. Brain Res Bull 43:473–483
Fuchs AF, Kaneko CR, Scudder CA (1985) Brainstem control of saccadic eye movements. Annu Rev Neurosci 8:307–337
Fuchs AF, Robinson FR, Straube A (1993) Role of the caudal fastigial nucleus in saccade generation. I. Neuronal discharge pattern. J Neurophysiol 70:1723–1740
Fuchs AF, Reiner D, Pong M (1996) Transfer of gain changes from targeting to other types of saccade in the monkey: constraints on possible sites of saccadic gain adaptation. J Neurophysiol 76:2522–2535
Fujita M (2005) Feed-forward associative learning for volitional movement control. Neurosci Res 52:153–165
Fujita M, Amagai A, Minakawa F, Aoki M (2002) Selective and delay adaptation of human saccades. Brain Res Cogn Brain Res 13:41–52
Gonzalo-Ruiz A, Leichnetz GR (1990) Afferents of the caudal fastigial nucleus in a new world monkey (Cebus apella). Exp Brain Res 80:600–608
Harting JK (1977) Descending pathways from the superior collicullus: an autoradiographic analysis in the rhesus monkey (Macaca mulatta). J Comp Neurol 173:583–612
Henson DB (1978) Corrective saccades—effects of altering visual feedback. Vis Res 18:63–67
Hopp JJ, Fuchs AF (2004) The characteristics and neuronal substrate of saccadic eye movement plasticity. Prog Neurobiol 72:27–53
Inaba N, Iwamoto Y, Yoshida K (2003) Changes in cerebellar fastigial burst activity related to saccadic gain adaptation in the monkey. Neurosci Res 46:359–368
Kaku Y, Yoshida K, Iwamoto Y (2009) Learning signals from the superior colliculus for adaptation of saccadic eye movements in the monkey. J Neurosci 29:5266–5275
Kawato M (1996) Learning internal models of the motor apparatus. In: Bloedel JR, Ebner TJ, Wise SP (eds) The acquisition of motor behaviors in vertebrates. MIT Press, Cambridge, MA, pp 409–430
Kleine JF, Guan Y, Büttner U (2003) Saccade-related neurons in the primate fastigial nucleus: what do they encode? J Neurophysiol 90:3137–3154
Kojima Y, Iwamoto Y, Yoshida K (2004) Memory of learning facilitates saccadic adaptation in the monkey. J Neurosci 25:7531–7539
Kojima Y, Iwamoto Y, Yoshida K (2005) Effect of saccadic amplitude adaptation on subsequent adaptation of saccades in different directions. Neurosci Res 53:404–412
Kojima Y, Yoshida K, Iwamoto Y (2007) Microstimulation of the midbrain tegmentum creates learning signals for saccade adaptation. J Neurosci 27:3759–3767
Kojima Y, Iwamoto Y, Robinson FR, Noto CT, Yoshida K (2008) Premotor inhibitory neurons carry signals related to saccade adaptation in the monkey. J Neurophysiol 99:220–230
Kojima Y, Soetedjo R, Fuchs AF (2010) Changes in simple spike activity of some Purkinje cells in the oculomotor vermis during saccade adaptation are appropriate to participate in motor learning. J Neurosci 30:3715–3727
Kommerell G, Olivier D, Theopold H (1976) Adaptive programming of phasic and tonic components in saccadic eye movements. Investigations of patients with abducens palsy. Invest Ophthalmol 15:657–660
Kröller J, Pélisson D, Prablanc C (1996) On the short-term adaptation of eye saccades and its transfer to head movements. Exp Brain Res 111:477–482
Kuki Y, Hirata Y, Blazquez PM, Heiney SA, Highstein SM (2004) Memory retention of vestibuloocular reflex motor learning in squirrel monkeys. Neuroreport 29:1007–1011
Kyuhou S-I, Matsuzaki R (1991) Topographical organization of the tectoolivo-cerebellar projection in the cat. Neuroscience 41:227–241
Leigh RJ, Zee DS (2006) A survey of eye movements: characteristics and teleology. In: The neurology of eye movements. Oxford University Press, New York, pp 3–19
Lewis RF, Zee DS, Gaymard BM, Guthrie BL (1994) Extraocular muscle proprioception functions in the control of ocular alignment and eye movement conjugacy. J Neurophysiol 71:1028–1031
Lewis RF, Zee DS, Hayman MR, Tamargo RJ (2001) Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles. Exp Brain Res 141:349–358
Li J, Smith SS, McElligott JG (1995) Cerebellar nitric oxide is necessary for vestibulo-ocular reflex adaptation, a sensorimotor model of learning. J Neurophysiol 74:489–494
Marr D (1969) A theory of cerebellar cortex. J Physiol (London) 202:437–470
Mauk MD, Steinmetz JE, Thompson RF (1986) Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci U S A 83:5349–5353
Mays LE, Sparks DL (1980) Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol 43:207–232
McLaughlin SC (1967) Parametric adjustment in saccadic eye movements. Percept Psychophys 2:359–362
Melis BJ, van Gisbergen JA (1996) Short-term adaptation of electrically induced saccades in monkey superior colliculus. J Neurophysiol 76:1744–1758
Miller JM, Anstis T, Templeton WB (1981) Saccadic plasticity: parametric adaptive control by retinal feedback. J Exp Psychol Hum Percept Perform 7:356–366
Miura M, Iwamoto Y, Yoshida K (2007) Long-term facilitation of saccade adaptation by repeated induction. Soc Neurosci Abstr 719.14
Moschovakis AK, Scudder CA, Highstein SM (1996) The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol 50:133–254
Noda H, Sugita S, Ikeda Y (1990) Afferent and efferent connections of the oculomotor region of the fastigial nucleus in the macaque monkey. J Comp Neurol 302:330–348
Noto CT, Robinson FR (2001) Visual error is the stimulus for saccade gain adaptation. Brain Res Cogn Brain Res 12:301–305
Noto CT, Watanabe S, Fuchs AF (1999) Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction. J Neurophysiol 81:2798–2813
Ohtsuka K, Noda H (1991) Saccadic burst neurons in the oculomotor region of the fastigial nucleus of macaque monkeys. J Neurophysiol 65:1422–1434
Ohtsuka K, Noda H (1995) Discharge properties of Purkinje cells in the oculomotor vermis during visually guided saccades in the macaque monkey. J Neurophysiol 74:1828–1840
Optican LM, Robinson DA (1980) Cerebellar-dependent adaptive control of primate saccadic system. J Neurophysiol 44:1058–1076
Panouillères M, Weiss T, Urquizar C, Salemme R, Munoz DP, Pélisson D (2009) Behavioral evidence of separate adaptation mechanisms controlling saccade amplitude lengthening and shortening. J Neurophysiol 101:1550–1559
Phillips JO, Fuchs AF, Ling L, Iwamoto Y, Votaw S (1997) Gain adaptation of eye and head movement components of simian gaze shifts. J Neurophysiol 78:2817–2821
Robinson FR, Fuchs AF (2001) The role of the cerebellum in voluntary eye movements. Annu Rev Neurosci 24:981–1004
Robinson FR, Noto CT (2005) Roll of the cerebellar oculomotor vermis in saccade adaptation. Soc Neurosci Abstr 986.4
Robinson FR, Straube A, Fuchs AF (1993) Role of the caudal fastigial nucleus in saccade generation. II. Effects of muscimol inactivation. J Neurophysiol 70:1741–1758
Robinson FR, Fuchs AF, Noto CT (2002) Cerebellar influences on saccade plasticity. Ann N Y Acad Sci 956:155–163
Robinson FR, Noto CT, Bevans SE (2003) Effect of visual error size on saccade adaptation in monkey. J Neurophysiol 90:1235–1244
Robinson FR, Soetedjo R, Noto CT (2006) Distinct short-term and long-term adaptation to reduce saccade size in monkey. J Neurophysiol 96:1030–1041
Schweighofer N, Arbib MA, Dominey PF (1996) A model of the cerebellum in adaptive control of saccadic gain. I. The model and its biological substrate. Biol Cybern 75:19–28
Scudder CA, McGee DM (2000) Connections of monkey saccade-related fastigial nucleus neurons revealed by anatomical and physiological methods. Soc Neurosci Abstr 971.26
Scudder CA, McGee DM (2003) Adaptive modification of saccade size produces correlated changes in the discharges of fastigial nucleus neurons. J Neurophysiol 90:1011–1026
Scudder CA, Batourina EY, Tunder GS (1998) Comparison of two methods of producing adaptation of saccade size and implications for the site of plasticity. J Neurophysiol 79:704–715
Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res 142:439–462
Semmlow JL, Gauthier GM, Vercher JL (1987) Short term adaptive modification of saccade amplitude. In: O’Regan J, Levy-Schoen A (eds) Eye movements: from physiology to cognition. Elsevier, Amsterdam, pp 191–200
Shafer JL, Noto CT, Fuchs AF (2000) Temporal characteristics of error signals driving saccadic gain adaptation in the macaque monkey. J Neurophysiol 84:88–95
Shutoh F, Ohki M, Kitazawa H, Itohara S, Nagao S (2006) Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 12:767–777
Snow R, Hore J, Vilis T (1985) Adaptation of saccadic and vestibulo-ocular systems after extraocular muscle tenectomy. Invest Ophthalmol Vis Sci 26:924–931
Soetedjo R, Fuchs AF (2006) Complex spike activity of Purkinje cells in the oculomotor vermis during behavioral adaptation of monkey saccades. J Neurosci 26:7741–7755
Soetedjo R, Kojima Y, Fuchs AF (2008) Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning? J Neurophysiol 100:1949–1966
Soetedjo R, Kojima Y, Fuchs AF (2009) Subthreshold activation of the superior colliculus drives saccade motor learning. J Neurosci 29:15213–15222
Sparks DL, Hartwich-Young R (1989) The deep layers of the superior SC. In: Wurtz RH, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 213–255
Straube A, Deubel H, Spuler A, Büttner U (1995) Differential effect of a bilateral deep cerebellar nuclei lesion on externally and internally triggered saccades in humans. Neuro-Ophthalmology 15:67–74
Straube A, Fuchs AF, Usher S, Robinson FR (1997) Characteristics of saccadic gain adaptation in rhesus macaques. J Neurophysiol 77:874–895
Takagi M, Zee DS, Tamargo RJ (1998) Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol 80:1911–1931
Takeichi N, Kaneko CR, Fuchs AF (2005) Discharge of monkey nucleus reticularis tegmenti pontis neurons changes during saccade adaptation. J Neurophysiol 94:1938–1951
Takeichi N, Kaneko CR, Fuchs AF (2007) Activity changes in monkey superior colliculus during saccade adaptation. J Neurophysiol 97:4096–4107
Thielert CD, Thier P (1993) Patterns of projections from the pontine nuclei and the nucleus reticularis tegmenti pontis to the posterior vermis in the rhesus monkey: a study using retrograde tracers. J Comp Neurol 337:113–126
Thier P, Dicke PW, Haas R, Barash S (2000) Encoding of movement time by populations of cerebellar Purkinje cells. Nature 405:72–76
Tian J, Ethier V, Shadmehr R, Fujita M, Zee DS (2009) Some perspectives on saccade adaptation. Ann N Y Acad Sci 1164:166–172
Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62
Waespe W, Müller-Meisser E (1996) Directional reversal of saccadic dysmetria and gain adaptivity in a patient with a superior cerebellar artery infarction. Neuro-Ophthalmology 16:65–74
Wallman J, Fuchs AF (1998) Saccadic gain modification: visual error drives motor adaptation. J Neurophysiol 80:2405–2416
Watanabe S, Noto CT, Fuchs AF (2000) Flexibility of saccade adaptation in the monkey: different gain states for saccades in the same direction. Exp Brain Res 130:169–176
Yamada J, Noda H (1987) Afferent and efferent connections of the oculomotor cerebellar vermis in the macaque monkey. J Comp Neurol 265:224–241
Zee DS, Yee RD, Cogan DG, Robinson DA, Engel WK (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234
Zhou W, Weldon P, Tang B, King WM (2003) Rapid motor learning in the translational vestibulo-ocular reflex. J Neurosci 15:4288–4298
Acknowledgments
We thank Masahiko Fujita for his comments on the earlier version of the manuscript and two anonymous reviewers for their constructive criticisms. We also thank Kozo Kobayashi for building laboratory facilities and the staff at the Corporation for Production and Research of Laboratory Primates for their help in surgery and veterinary care of our monkeys. We are grateful to Flaminia Miyamasu for her grammatical revision of the text.
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Iwamoto, Y., Kaku, Y. Saccade adaptation as a model of learning in voluntary movements. Exp Brain Res 204, 145–162 (2010). https://doi.org/10.1007/s00221-010-2314-3
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DOI: https://doi.org/10.1007/s00221-010-2314-3