Skip to main content
SpringerLink
Log in

The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning

  • Review
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

The cerebellum is essential for error-driven motor learning and is strongly implicated in detecting and correcting for motor errors. Therefore, elucidating how motor errors are represented in the cerebellum is essential in understanding cerebellar function, in general, and its role in motor learning, in particular. This review examines how motor errors are encoded in the cerebellar cortex in the context of a forward internal model that generates predictions about the upcoming movement and drives learning and adaptation. In this framework, sensory prediction errors, defined as the discrepancy between the predicted consequences of motor commands and the sensory feedback, are crucial for both on-line movement control and motor learning. While many studies support the dominant view that motor errors are encoded in the complex spike discharge of Purkinje cells, others have failed to relate complex spike activity with errors. Given these limitations, we review recent findings in the monkey showing that complex spike modulation is not necessarily required for motor learning or for simple spike adaptation. Also, new results demonstrate that the simple spike discharge provides continuous error signals that both lead and lag the actual movements in time, suggesting errors are encoded as both an internal prediction of motor commands and the actual sensory feedback. These dual error representations have opposing effects on simple spike discharge, consistent with the signals needed to generate sensory prediction errors used to update a forward internal model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Marr D. A theory of cerebellar cortex. J Physiol. 1969;202:437–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Albus JS. A theory of cerebellar function. Math Biosci. 1971;10:25–61.

    Article  Google Scholar 

  3. Ito M, Kano M. Long-lasting depression of parallel fiber-Purkinje cell transmission induced by conjunctive stimulation of parallel fibers and climbing fibers in the cerebellar cortex. Neurosci Lett. 1982;33:253–8.

    Article  CAS  PubMed  Google Scholar 

  4. Todorov E, Jordan MI. Optimal feedback control as a theory of motor coordination. Nat Neurosci. 2002;5:1226–35.

    Article  CAS  PubMed  Google Scholar 

  5. Berniker M, Kording K. Estimating the sources of motor errors for adaptation and generalization. Nat Neurosci. 2008;11:1454–61.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Shadmehr R, Smith MA, Krakauer JW. Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci. 2010;33:89–108.

    Article  CAS  PubMed  Google Scholar 

  7. Wolpert DM, Ghahramani Z. Computational principles of movement neuroscience. Nat Neurosci. 2000;3(Suppl):1212–7.

    Article  CAS  PubMed  Google Scholar 

  8. Miall RC, Wolpert DM. Forward models for physiological motor control. Neural Netw. 1996;9:1265–79.

    Article  PubMed  Google Scholar 

  9. Kawato M. Internal models for motor control and trajectory planning. Curr Opin Neurobiol. 1999;9:718–27.

    Article  CAS  PubMed  Google Scholar 

  10. Wolpert DM, Ghahramani Z, Jordan MI. An internal model for sensorimotor integration. Science. 1995;269:1880–2.

    Article  CAS  PubMed  Google Scholar 

  11. Morton SM, Bastian AJ. Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci. 2006;26:9107–16.

    Article  CAS  PubMed  Google Scholar 

  12. Robinson DA. Oculomotor control signals. In: Bachyrita P, Lennerstrand G, editors. Basic mechanisms of ocular motility and their clinical implications. Oxford: Pergamon; 1975. p. 337–74.

    Google Scholar 

  13. Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R. Cerebellar contributions to adaptive control of saccades in humans. J Neurosci. 2009;29:12930–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Maschke M, Gomez CM, Ebner TJ, Konczak J. Hereditary cerebellar ataxia progressively impairs force adaptation during goal-directed arm movements. J Neurophysiol. 2004;91:230–8.

    Article  PubMed  Google Scholar 

  15. Imamizu H, Miyauchi S, Tamada T, et al. Human cerebellar activity reflecting an acquired internal model of a new tool. Nature. 2000;403:192–5.

    Article  CAS  PubMed  Google Scholar 

  16. Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R. Neural correlates of reach errors. J Neurosci. 2005;25:9919–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Flanagan JR, Wing AM. The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J Neurosci. 1997;17:1519–28.

    CAS  PubMed  Google Scholar 

  18. Bell CC, Han V, Sawtell NB. Cerebellum-like structures and their implications for cerebellar function. Annu Rev Neurosci. 2008;31:1–24.

    Article  CAS  PubMed  Google Scholar 

  19. Brooks JX, Cullen KE. The primate cerebellum selectively encodes unexpected self-motion. Curr Biol. 2013;23:947–55.

    Article  CAS  PubMed  Google Scholar 

  20. Wong AL, Shelhamer M. Sensorimotor adaptation error signals are derived from realistic predictions of movement outcomes. J Neurophysiol. 2011;105:1130–40.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Mazzoni P, Krakauer JW. An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci. 2006;26:3642–5.

    Article  CAS  PubMed  Google Scholar 

  22. Taylor JA, Ivry RB. The role of strategies in motor learning. Ann N Y Acad Sci. 2012;1241:1–12.

    Article  Google Scholar 

  23. Izawa J, Criscimagna-Hemminger SE, Shadmehr R. Cerebellar contributions to reach adaptation and learning sensory consequences of action. J Neurosci. 2012;32:4230–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gaveau V, Prablanc C, Laurent D, Rossetti Y, Priot AE. Visuomotor adaptation needs a validation of prediction error by feedback error. Front Hum Neurosci. 2014;8:880.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Henriques DYP, Cressman EK. Visuomotor adaptation and proprioceptive recalibration. J Mot Behav. 2012;44:435–44.

    Article  PubMed  Google Scholar 

  26. Simani MC, McGuire LM, Sabes PN. Visual-shift adaptation is composed of separable sensory and task-dependent effects. J Neurophysiol. 2007;98:2827–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. van Beers RJ, Wolpert DM, Haggard P. When feeling is more important than seeing in sensorimotor adaptation. Curr Biol. 2002;12:834–7.

    Article  PubMed  Google Scholar 

  28. Kawato M. Learning internal models of the motor apparatus. In: Bloedel JR, Ebner TJ, Wise SP, editors. The acquisition of motor behavior in vertebrates. Cambridge: MIT Press; 1996. p. 409–30.

    Google Scholar 

  29. Miles FA, Lisberger SG. The “error” signals subserving adaptive gain control in the primate vestibulo-ocular reflex. Ann N Y Acad Sci. 1981;374:513–25.

    Article  CAS  PubMed  Google Scholar 

  30. Magescas F, Prablanc C. Automatic drive of limb motor plasticity. J Cogn Neurosci. 2006;18:75–83.

    Article  CAS  PubMed  Google Scholar 

  31. Cameron BD, Franks IM, Inglis JT, Chua R. Reach adaptation to explicit vs. implicit target error. Exp Brain Res. 2010;203:367–80.

    Article  PubMed  Google Scholar 

  32. Izawa J, Shadmehr R. Learning from sensory and reward prediction errors during motor adaptation. PLoS Comput Biol. 2011;7, e1002012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Schonberg T, Daw ND, Joel D, O'Doherty JP. Reinforcement learning signals in the human striatum distinguish learners from nonlearners during reward-based decision making. J Neurosci. 2007;27:12860–7.

    Article  CAS  PubMed  Google Scholar 

  34. Redding GM, Wallace B. Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform. 1996;22:379–94.

    Article  CAS  PubMed  Google Scholar 

  35. Cressman EK, Henriques DY. Reach adaptation and proprioceptive recalibration following exposure to misaligned sensory input. J Neurophysiol. 2010;103:1888–95.

    Article  PubMed  Google Scholar 

  36. Held R, Freedman SJ. Plasticity in human sensorimotor control. Science. 1963;142:455–62.

    Article  CAS  PubMed  Google Scholar 

  37. Pasalar S, Roitman AV, Durfee WK, Ebner TJ. Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci. 2006;9:1404–11.

    Article  CAS  PubMed  Google Scholar 

  38. Bastian AJ. Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol. 2006;16:645–9.

    Article  CAS  PubMed  Google Scholar 

  39. Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2:338–47.

    Article  CAS  PubMed  Google Scholar 

  40. Shadmehr R, Holcomb HH. Neural correlates of motor memory consolidation. Science. 1997;277:821–5.

    Article  CAS  PubMed  Google Scholar 

  41. Kawato M, Kuroda T, Imamizu H, Nakano E, Miyauchi S, Yoshioka T. Internal forward models in the cerebellum: fMRI study on grip force and load force coupling. Prog Brain Res. 2003;142:171–88.

    Article  PubMed  Google Scholar 

  42. Krakauer JW, Ghilardi MF, Mentis M, et al. Differential cortical and subcortical activations in learning rotations and gains for reaching: a PET study. J Neurophysiol. 2004;91:924–33.

    Article  PubMed  Google Scholar 

  43. Takagi M, Zee DS, Tamargo RJ. Effects of lesions of the oculomotor cerebellar vermis on eye movements in primate: smooth pursuit. J Neurophysiol. 2000;83:2047–62.

    CAS  PubMed  Google Scholar 

  44. Golla H, Tziridis K, Haarmeier T, Catz N, Barash S, Thier P. Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease. Eur J Neurosci. 2008;27:132–44.

    Article  PubMed  Google Scholar 

  45. Muller F, Dichgans J. Impairments of precision grip in two patients with acute unilateral cerebellar lesions: a simple parametric test for clinical use. Neuropsychologia. 1994;32:265–9.

    Article  CAS  PubMed  Google Scholar 

  46. Nowak DA, Hermsdorfer J, Rost K, Timmann D, Topka H. Predictive and reactive finger force control during catching in cerebellar degeneration. Cerebellum. 2004;3:227–35.

    Article  PubMed  Google Scholar 

  47. Smith MA, Shadmehr R. Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol. 2005;93:2809–21.

    Article  PubMed  Google Scholar 

  48. Ito M. Cerebellar learning in the vestibulo-ocular reflex. Trends Cogn Sci. 1998;2:313–21.

    Article  CAS  PubMed  Google Scholar 

  49. Ito M. Cerebellar long-term depression: characterization, signal transduction, and functional roles. Physiol Rev. 2001;81:1143–95.

    CAS  PubMed  Google Scholar 

  50. Prsa M, Thier P. The role of the cerebellum in saccadic adaptation as a window into neural mechanisms of motor learning. Eur J Neurosci. 2011;33:2114–28.

    Article  PubMed  Google Scholar 

  51. Thompson RF, Steinmetz JE. The role of the cerebellum in classical conditioning of discrete behavioral responses. Neuroscience. 2009;162:732–55.

    Article  CAS  PubMed  Google Scholar 

  52. Thier P, Ilg U. The neural basis of smooth-pursuit eye movements. Curr Opin Neurobiol. 2005;15:645–52.

    Article  CAS  PubMed  Google Scholar 

  53. Tseng YW, Diedrichsen J, Krakauer JW, Shadmehr R, Bastian AJ. Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol. 2007;98:54–62.

    Article  PubMed  Google Scholar 

  54. Schlerf JE, Ivry RB, Diedrichsen J. Encoding of sensory prediction errors in the human cerebellum. J Neurosci. 2012;32:4913–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Taylor JA, Klemfuss NM, Ivry RB. An explicit strategy prevails when the cerebellum fails to compute movement errors. Cerebellum. 2010;9:580–6.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Oscarsson O. Functional organization of olivary projection to the cerebellar anterior lobe. In: Courville J, editor. The inferior olivary nucleus: anatomy and physiology. New York: Raven; 1980. p. 279–90.

    Google Scholar 

  57. Gilbert PF, Thach WT. Purkinje cell activity during motor learning. Brain Res. 1977;128:309–28.

    Article  CAS  PubMed  Google Scholar 

  58. Ito M. Mechanisms of motor learning in the cerebellum. Brain Res. 2000;886:237–45.

    Article  CAS  PubMed  Google Scholar 

  59. Stone LS, Lisberger SG. Detection of tracking errors by visual climbing fiber inputs to monkey cerebellar flocculus during pursuit eye movements. Neurosci Lett. 1986;72:163–8.

    Article  CAS  PubMed  Google Scholar 

  60. Kawato M, Gomi H. A computational model of four regions of the cerebellum based on feedback-error learning. Biol Cybern. 1992;68:95–103.

    Article  CAS  PubMed  Google Scholar 

  61. Kitazawa S, Kimura T, Yin PB. Cerebellar complex spikes encode both destinations and errors in arm movements. Nature. 1998;392:494–7.

    Article  CAS  PubMed  Google Scholar 

  62. Ito M. Error detection and representation in the olivo-cerebellar system. Front Neural Circuits. 2013;7:1–8.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Graf W, Simpson JI, Leonard CS. Spatial organization of visual messages of the rabbit’s cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol. 1988;60:2091–121.

    CAS  PubMed  Google Scholar 

  64. Kobayashi Y, Kawano K, Takemura A, et al. Temporal firing patterns of Purkinje cells in the cerebellar ventral paraflocculus during ocular following responses in monkeys II. Complex spikes. J Neurophysiol. 1998;80:832–48.

    CAS  PubMed  Google Scholar 

  65. Barmack NH, Shojaku H. Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J Neurophysiol. 1995;74:2573–89.

    CAS  PubMed  Google Scholar 

  66. Stone LS, Lisberger SG. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. II. Complex spikes. J Neurophysiol. 1990;63:1262–75.

    CAS  PubMed  Google Scholar 

  67. Kim JH, Wang JJ, Ebner TJ. Climbing fiber afferent modulation during treadmill locomotion in the cat. J Neurophysiol. 1987;57:787–802.

    CAS  PubMed  Google Scholar 

  68. Lou JS, Bloedel JR. The responses of simultaneously recorded Purkinje cells to the perturbations of the step cycle in the walking ferret: a study using a new analytical method—the real-time postsynaptic response (RTPR). Brain Res. 1986;365:340–4.

    Article  CAS  PubMed  Google Scholar 

  69. Andersson G, Armstrong DM. Complex spikes in Purkinje cells in the lateral vermis (b zone) of the cat cerebellum during locomotion. J Physiol. 1987;385:107–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Soetedjo R, Fuchs AF. Complex spike activity of Purkinje cells in the oculomotor vermis during behavioral adaptation of monkey saccades. J Neurosci. 2006;26:7741–55.

    Article  CAS  PubMed  Google Scholar 

  71. Soetedjo R, Kojima Y, Fuchs AF. Complex spike activity in the oculomotor vermis of the cerebellum: a vectorial error signal for saccade motor learning? J Neurophysiol. 2008;100:1949–66.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Marko MK, Haith AM, Harran MD, Shadmehr R. Sensitivity to prediction error in reach adaptation. J Neurophysiol. 2012;108:1752–63.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Robinson FR, Noto CT, Bevans SE. Effect of visual error size on saccade adaptation in monkey. J Neurophysiol. 2003;90:1235–44.

    Article  PubMed  Google Scholar 

  74. Wei K, Kording K. Relevance of error: what drives motor adaptation? J Neurophysiol. 2009;101:655–64.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Miles FA, Lisberger SG. Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu Rev Neurosci. 1981;4:273–99.

    Article  CAS  PubMed  Google Scholar 

  76. Boyden ES, Raymond JL. Active reversal of motor memories reveals rules governing memory encoding. Neuron. 2003;39:1031–42.

    Article  CAS  PubMed  Google Scholar 

  77. Boyden ES, Katoh A, Raymond JL. Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci. 2004;27:581–609.

    Article  CAS  PubMed  Google Scholar 

  78. Medina JF, Lisberger SG. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat Neurosci. 2008;11:1185–92.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Yang Y, Lisberger SG. Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration. Nature. 2014;510:529–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ojakangas CL, Ebner TJ. Purkinje cell complex and simple spike changes during a voluntary arm movement learning task in the monkey. J Neurophysiol. 1992;68:2222–36.

    CAS  PubMed  Google Scholar 

  81. Ojakangas CL, Ebner TJ. Purkinje cell complex spike activity during voluntary motor learning: relationship to kinematics. J Neurophysiol. 1994;72:2617–30.

    CAS  PubMed  Google Scholar 

  82. Rasmussen A, Jirenhed DA, Zucca R, Johansson F, Svensson P, Hesslow G. Number of spikes in climbing fibers determines the direction of cerebellar learning. J Neurosci. 2013;33:13436–40.

    Article  CAS  PubMed  Google Scholar 

  83. De Zeeuw CI, Yeo CH. Time and tide in cerebellar memory formation. Curr Opin Neurobiol. 2005;15:667–74.

    Article  PubMed  CAS  Google Scholar 

  84. Yeo CH, Hardiman MJ, Glickstein M. Classical conditioning of the nictitating membrane response of the rabbit. II. Lesions of the cerebellar cortex. Exp Brain Res. 1985;60:99–113.

    Article  CAS  PubMed  Google Scholar 

  85. Mauk MD, Steinmetz JE, Thompson RF. Classical conditioning using stimulation of the inferior olive as the unconditioned stimulus. Proc Natl Acad Sci U S A. 1986;83:5349–53.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Welsh JP. Systemic harmaline blocks associative and motor learning by the actions of the inferior olive. Eur J Neurosci. 1998;10:3307–20.

    Article  CAS  PubMed  Google Scholar 

  87. Ghelarducci B, Ito M, Yagi N. Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res. 1975;87:66–72.

    Article  CAS  PubMed  Google Scholar 

  88. Ohyama T, Nores WL, Murphy M, Mauk MD. What the cerebellum computes. Trends Neurosci. 2003;26:222–7.

    Article  CAS  PubMed  Google Scholar 

  89. Ebner TJ, Johnson MT, Roitman A, Fu Q. What do complex spikes signal about limb movements? Ann NY Acad Sci. 2002;978:205–18.

    Article  PubMed  Google Scholar 

  90. Fu QG, Mason CR, Flament D, Coltz JD, Ebner TJ. Movement kinematics encoded in complex spike discharge of primate cerebellar Purkinje cells. NeuroReport. 1997;8:523–9.

    Article  CAS  PubMed  Google Scholar 

  91. Horn KM, van Kan PL, Gibson AR. Reduction of rostral dorsal accessory olive responses during reaching. J Neurophysiol. 1996;76:4140–51.

    CAS  PubMed  Google Scholar 

  92. Catz N, Dicke PW, Thier P. Cerebellar complex spike firing is suitable to induce as well as to stabilize motor learning. Curr Biol. 2005;15:2179–89.

    Article  CAS  PubMed  Google Scholar 

  93. Dash S, Catz N, Dicke PW, Thier P. Specific vermal complex spike responses build up during the course of smooth-pursuit adaptation, paralleling the decrease of performance error. Exp Brain Res. 2010;205:41–55.

    Article  PubMed  Google Scholar 

  94. Ebner TJ, Hewitt A, Popa LS. What features of movements are encoded in the discharge of cerebellar neurons during limb movements? Cerebellum. 2011;10:683–93.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Najafi F, Giovannucci A, Wang SS, Medina JF. Sensory-driven enhancement of calcium signals in individual Purkinje cell dendrites of awake mice. Cell Rep. 2014;6:792–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Najafi F, Giovannucci A, Wang SS, Medina JF. Coding of stimulus strength via analog calcium signals in Purkinje cell dendrites of awake mice. Elife. 2014;3, e03663.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  97. Welsh JP, Lang EJ, Suglhara I, Llinas R. Dynamic organization of motor control within the olivocerebellar system. Nature. 1995;374:453–7.

    Article  CAS  PubMed  Google Scholar 

  98. Lang EJ. Excitatory afferent modulation of complex spike synchrony. Cerebellum. 2003;2:165–70.

  99. Ozden I, Dombeck DA, Hoogland TM, Tank DW, Wang SS. Widespread state-dependent shifts in cerebellar activity in locomoting mice. PLoS ONE. 2012;7, e42650.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Sasaki K, Bower JM, Llinas R. Multiple Purkinje cell recording in rodent cerebellar cortex. Eur J Neurosci. 1989;1:572–86.

    Article  PubMed  Google Scholar 

  101. Lou JS, Bloedel JR. Responses of sagittally aligned Purkinje cells during perturbed locomotion: synchronous activation of climbing fiber inputs. J Neurophysiol. 1992;68:570–80.

    CAS  PubMed  Google Scholar 

  102. Jacobson GA, Lev I, Yarom Y, Cohen D. Invariant phase structure of olivo-cerebellar oscillations and its putative role in temporal pattern generation. Proc Natl Acad Sci U S A. 2009;106:3579–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Schweighofer N, Doya K, Fukai H, Chiron JV, Furukawa T, Kawato M. Chaos may enhance information transmission in the inferior olive. Proc Natl Acad Sci U S A. 2004;101:4655–60.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Kimpo RR, Rinaldi JM, Kim CK, Payne HL, Raymond JL. Gating of neural error signals during motor learning. Elife. 2014;3, e02076.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Nguyen-Vu TD, Kimpo RR, Rinaldi JM, et al. Cerebellar Purkinje cell activity drives motor learning. Nat Neurosci. 2013;16:1734–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Guo CC, Ke MC, Raymond JL. Cerebellar encoding of multiple candidate error cues in the service of motor learning. J Neurosci. 2014;34:9880–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Ke MC, Guo CC, Raymond JL. Elimination of climbing fiber instructive signals during motor learning. Nat Neurosci. 2009;12:1171–9.

    Article  CAS  PubMed  Google Scholar 

  108. Shin SL, Zhao GQ, Raymond JL. Signals and learning rules guiding oculomotor plasticity. J Neurosci. 2014;34:10635–44.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Greger B, Norris S. Simple spike firing in the posterior lateral cerebellar cortex of Macaque Mulatta was correlated with success-failure during a visually guided reaching task. Exp Brain Res. 2005;167:660–5.

    Article  PubMed  Google Scholar 

  110. Roitman AV, Pasalar S, Ebner TJ. Single trial coupling of Purkinje cell activity to speed and error signals during circular manual tracking. Exp Brain Res. 2009;192:241–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Kahlon M, Lisberger SG. Changes in the responses of Purkinje cells in the floccular complex of monkeys after motor learning in smooth pursuit eye movements. J Neurophysiol. 2000;84:2945–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  112. Hewitt A, Popa LS, Pasalar S, Hendrix CM, Ebner TJ. Representation of limb kinematics in Purkinje cell simple spike discharge is conserved across multiple tasks. J Neurophysiol. 2011;106:2232–47.

    Article  PubMed  PubMed Central  Google Scholar 

  113. Popa LS, Hewitt AL, Ebner TJ. Predictive and feedback performance errors are signaled in the simple spike discharge of individual Purkinje cells. J Neurosci. 2012;32:15345–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Paninski L, Fellows MR, Hatsopoulos NG, Donoghue JP. Spatiotemporal tuning of motor cortical neurons for hand position and velocity. J Neurophysiol. 2004;91:515–32.

    Article  PubMed  Google Scholar 

  115. Popa LS, Hewitt AL, Ebner TJ. The cerebellum for jocks and nerds alike. Front Syst Neurosci. 2014;8:1–13.

    Article  Google Scholar 

  116. Crowe DA, Goodwin SJ, Blackman RK, et al. Prefrontal neurons transmit signals to parietal neurons that reflect executive control of cognition. Nat Neurosci. 2013;16:1484–91.

    Article  CAS  PubMed  Google Scholar 

  117. Wallman J, Fuchs AF. Saccadic gain modification: visual error drives motor adaptation. J Neurophysiol. 1998;80:2405–16.

    CAS  PubMed  Google Scholar 

  118. Noto CT, Robinson FR. Visual error is the stimulus for saccade gain adaptation. Brain Res Cogn Brain Res. 2001;12:301–5.

    Article  CAS  PubMed  Google Scholar 

  119. Nezafat R, Shadmehr R, Holcomb HH. Long-term adaptation to dynamics of reaching movements: a PET study. Exp Brain Res. 2001;140:66–76.

    Article  CAS  PubMed  Google Scholar 

  120. Balsters JH, Ramnani N. Cerebellar plasticity and the automation of first-order rules. J Neurosci. 2011;31:2305–12.

    Article  CAS  PubMed  Google Scholar 

  121. Ploghaus A, Tracey I, Clare S, Gati JS, Rawlins JN, Matthews PM. Learning about pain: the neural substrate of the prediction error for aversive events. Proc Natl Acad Sci U S A. 2000;97:9281–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Meyer-Lohmann J, Hore J, Brooks VB. Cerebellar participation in generation of prompt arm movements. J Neurophysiol. 1977;40:1038–50.

    CAS  PubMed  Google Scholar 

  123. Lisberger SG, Fuchs AF. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol. 1978;41:733–63.

    CAS  PubMed  Google Scholar 

  124. Jirenhed DA, Bengtsson F, Hesslow G. Acquisition, extinction, and reacquisition of a cerebellar cortical memory trace. J Neurosci. 2007;27:2493–502.

    Article  CAS  PubMed  Google Scholar 

  125. Catz N, Dicke PW, Thier P. Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response. Proc Natl Acad Sci U S A. 2008;105:7309–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Medina JF, Lisberger SG. Encoding and decoding of learned smooth pursuit eye movements in the floccular complex of the monkey cerebellum. J Neurophysiol. 2009;102:2039–54.

    Article  PubMed  PubMed Central  Google Scholar 

  127. Dash S, Dicke PW, Thier P. A vermal Purkinje cell simple spike population response encodes the changes in eye movement kinematics due to smooth pursuit adaptation. Front Syst Neurosci. 2013;7:3.

    PubMed  PubMed Central  Google Scholar 

  128. Hewitt AL, Popa LS, Ebner TJ. Changes in Purkinje cell simple spike encoding of reach kinematics during adaptation to a mechanical perturbation. J Neurosci. 2015;35:1106–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Dugas C, Smith AM. Responses of cerebellar Purkinje cells to slip of a hand-held object. J Neurophysiol. 1992;67:483–95.

    CAS  PubMed  Google Scholar 

  130. Nowak DA, Topka H, Timmann D, Boecker H, Hermsdorfer J. The role of the cerebellum for predictive control of grasping. Cerebellum. 2007;6:7–17.

    Article  PubMed  Google Scholar 

  131. Shadmehr R, Mussa-Ivaldi FA. Adaptive representation of dynamics during learning of a motor task. J Neurosci. 1994;14:3208–24.

    CAS  PubMed  Google Scholar 

  132. Krakauer JW, Pine ZM, Ghilardi MF, Ghez C. Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci. 2000;20:8916–24.

    CAS  PubMed  Google Scholar 

  133. Scheidt RA, Reinkensmeyer DJ, Conditt MA, Rymer WZ, Mussa-Ivaldi FA. Persistence of motor adaptation during constrained, multi-joint, arm movements. J Neurophysiol. 2000;84:853–62.

    CAS  PubMed  Google Scholar 

  134. Richter S, Maschke M, Timmann D, et al. Adaptive motor behavior of cerebellar patients during exposure to unfamiliar external forces. J Mot Behav. 2004;36:28–38.

    Article  PubMed  Google Scholar 

  135. Kojima Y, Soetedjo R, Fuchs AF. 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. 2010;30:3715–27.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Miles FA, Braitman DJ, Dow BM. Long-term adaptive changes in primate vestibuloocular reflex. IV. Electrophysiological observations in flocculus of adapted monkeys. J Neurophysiol. 1980;43:1477–93.

    CAS  PubMed  Google Scholar 

  137. Raymond JL, Lisberger SG. Multiple subclasses of Purkinje cells in the primate floccular complex provide similar signals to guide learning in the vestibulo-ocular reflex. Learn Mem. 1997;3:503–18.

    Article  CAS  PubMed  Google Scholar 

  138. Koekkoek SK, Hulscher HC, Dortland BR, et al. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science. 2003;301:1736–9.

    Article  CAS  PubMed  Google Scholar 

  139. Gao Z, van Beugen BJ, De Zeeuw CI. Distributed synergistic plasticity and cerebellar learning. Nat Rev Neurosci. 2012;13:619–35.

    Article  CAS  PubMed  Google Scholar 

  140. Hansel C, Linden DJ, D'Angelo E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat Neurosci. 2001;4:467–75.

    CAS  PubMed  Google Scholar 

  141. Jorntell H, Hansel C. Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron. 2006;52:227–38.

    Article  PubMed  CAS  Google Scholar 

  142. Sing GC, Joiner WM, Nanayakkara T, Brayanov JB, Smith MA. Primitives for motor adaptation reflect correlated neural tuning to position and velocity. Neuron. 2009;64:575–89.

    Article  CAS  PubMed  Google Scholar 

  143. Bauswein E, Kolb FP, Leimbeck B, Rubia FJ. Simple and complex spike activity of cerebellar Purkinje cells during active and passive movements in the awake monkey. J Physiol. 1983;339:379–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Mano N, Kanazawa I, Yamamoto K. Complex-spike activity of cerebellar Purkinje cells related to wrist tracking movement in monkey. J Neurophysiol. 1986;56:137–58.

    CAS  PubMed  Google Scholar 

  145. Roitman AV, Pasalar S, Johnson MT, Ebner TJ. Position, direction of movement, and speed tuning of cerebellar Purkinje cells during circular manual tracking in monkey. J Neurosci. 2005;25:9244–57.

    Article  CAS  PubMed  Google Scholar 

  146. Ramnani N. Automatic and controlled processing in the corticocerebellar system. Prog Brain Res. 2014;210:255–85.

    Article  PubMed  Google Scholar 

  147. Wolpert DM, Kawato M. Multiple paired forward and inverse models for motor control. Neural Netw. 1998;11:1317–29.

    Article  CAS  PubMed  Google Scholar 

  148. Krakauer JW, Ghilardi MF, Ghez C. Independent learning of internal models for kinematic and dynamic control of reaching. Nat Neurosci. 1999;2:1026–31.

    Article  CAS  PubMed  Google Scholar 

  149. Ebner TJ, Pasalar S. Cerebellum predicts the future motor state. Cerebellum. 2008;7:583–8.

    Article  PubMed  PubMed Central  Google Scholar 

  150. Cerminara NL, Apps R, Marple-Horvat DE. An internal model of a moving visual target in the lateral cerebellum. J Physiol. 2009;587:429–42.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. Witter L, Canto CB, Hoogland TM, de Gruijl JR, De Zeeuw CI. Strength and timing of motor responses mediated by rebound firing in the cerebellar nuclei after Purkinje cell activation. Front Neural Circuits. 2013;7:133.

    Article  PubMed  PubMed Central  Google Scholar 

  152. Chaumont J, Guyon N, Valera AM, et al. Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc Natl Acad Sci U S A. 2013;110:16223–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Marshall SP, Lang EJ. Local changes in the excitability of the cerebellar cortex produce spatially restricted changes in complex spike synchrony. J Neurosci. 2009;29:14352–62.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Yang Y, Lisberger SG. Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning. Elife. 2013;2, e01574.

    PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We wish to thank Lijuan Zhou for technical support and Kris Bettin for manuscript preparation. Supported in part by NIH grants R01 NS18338 and T32 GM008471 and NSF grant IGERT DGE-1069104.

Conflict of Interest Statement

There are no current or potential conflicts of interest for the four authors, Laurentiu S. Popa, Martha L. Streng, Angela L. Hewitt, and Timothy J. Ebner

Author information

Authors and Affiliations

  1. Department of Neuroscience, University of Minnesota, Lions Research Building, Room 421, 2001 Sixth St. S.E., Minneapolis, MN, 55455, USA

    Laurentiu S. Popa, Martha L. Streng, Angela L. Hewitt & Timothy J. Ebner

Authors
  1. Laurentiu S. Popa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martha L. Streng
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Angela L. Hewitt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Timothy J. Ebner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Timothy J. Ebner.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Popa, L.S., Streng, M.L., Hewitt, A.L. et al. The Errors of Our Ways: Understanding Error Representations in Cerebellar-Dependent Motor Learning. Cerebellum 15, 93–103 (2016). https://doi.org/10.1007/s12311-015-0685-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-015-0685-5

Keywords

Search

Navigation