Clinical Neuro-Cybernetics: Motor Learning in Neuronal Systems

  • Florian P. KolbEmail author
  • Dagmar Timmann
Part of the Topics in Biomedical Engineering International Book Series book series (ITBE)


Although the understanding of complex cerebellar function is still a matter of discussion, new imaging techniques have provided evidence that the human cerebellum is critically involved in motor learning. For associative plastic motor processes this evidence has been obtained by comparison of classically conditioned eyeblink results from cerebellar patients with those from corresponding control subjects, the former showing typically reduced incidence levels of conditioned responses. Of particular interest was that nonassociative-motor-related processes such as habituation are also affected characteristically in cerebellar patients. Aside from these motor-related functions, we also review evidence that the cerebellum may be involved as well in non-motor visuomotor associative learning. The common denominator for impaired function may be an inadequate error-detection or error-correction capability, a putative function of the olivo-cerebellar system. In the final section of this chapter, we review computational models based on feedback-error learning.


Conditioning Stimulus Purkinje Cell Unconditioned Stimulus Motor Learning Classical Conditioning 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

6. References

  1. 1.
    Adams JA. 1987. Historical review and appraisal of research on the learning retention, and transfer of human motor skills. Psychol Bull 101(1):41–74.CrossRefGoogle Scholar
  2. 2.
    Albus JS. 1971. A theory of cerebellar function. Math Biosci 10:25–61.CrossRefGoogle Scholar
  3. 3.
    Allen GI, Tsukahara N. 1974. Cerebrocerebellar communication systems. Physiol Rev 54:957–1006.PubMedGoogle Scholar
  4. 4.
    Amarenco P, Hauw JJ, Caplan LR. 1993. Cerebellar infarctions. In Handbook of cerebellar diseases, pp. 251–290. Ed. R Lechtenberg. Marcel Dekker, New York.Google Scholar
  5. 5.
    Arbib MA, Schweighofer N, Thach WT. 1995. Modeling of the cerebellum: from adaptation to coordination. In Motor control and sensory motor integration: issues and directions, pp. 11–36. Ed. DJ Glencross, JP Pick. Elsevier, Amsterdam.Google Scholar
  6. 6.
    Barlow JS. 2002. The cerebellum and adaptive control. Cambridge UP, Cambridge.Google Scholar
  7. 7.
    Bauswein E, Kolb FP, Leimbeck B, Rubia FJ. 1983. Simple and complex spike activity of cerebellar Purkinje cells during active and passive movements in the awake monkey. J Physiol 339:379–394.PubMedGoogle Scholar
  8. 8.
    Bloedel JR, Bracha V, Kelly TM, Wu JZ. 1991. Substrates for motor learning: does the cerebellum do it all? In Activity-driven CNS changes in learning and development, pp. 305–318. Ed. JR Wolpaw, JT Schmidt, TM Vaughan. New York Academy of Sciences, New York.Google Scholar
  9. 9.
    Bloedel JR, Bracha V. 1995. On the cerebellum, cutaneomuscular reflexes, movement control and the elusive engrams of memory. Behav Brain Res 68:1–44.PubMedCrossRefGoogle Scholar
  10. 10.
    Bracha V, Zhao L, Irwin KB, Bloedel JR. 2000. The human cerebellum and associative learning: dissociation between the acquisition, retention and extinction of conditioned eyeblinks. Brain Res 860:87–94.PubMedCrossRefGoogle Scholar
  11. 11.
    Bracha V, Webster ML, Winters NK, Irwin KB, Bloedel JR. 1994. Effects of muscimol inactivation of the cerebellar interposed-dentate nuclear complex on the performance of the nictitating membrane response in the rabbit. Exp Brain Res 100:453–468.PubMedGoogle Scholar
  12. 12.
    Braitenberg V, Atwood RP. 1958. Morphological observations on the cerebellar cortex. J Comp Neurol 109:1–33.PubMedCrossRefGoogle Scholar
  13. 13.
    Brindley GS. 1964. The use made by the cerebellum of the information that it receives from sense organs. Ibro Bull 3:80.Google Scholar
  14. 14.
    Brodal P. 1998. The central nervous system: structure and function, 2nd ed. Oxford UP, New York.Google Scholar
  15. 15.
    Canavan AG, Sprengelmeyer R, Diener HC, Homberg V. 1994. Conditional associative learning is impaired in cerebellar disease in humans. Behav Neurosci 108:1–11.CrossRefGoogle Scholar
  16. 16.
    Chambers WW, Sprague JM. 1955. Functional localization in the cerebellum, I: organization in longitudinal cortico-nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. J Comp Neurol 103:105–129.PubMedCrossRefGoogle Scholar
  17. 17.
    Daum I, Schugens MM, Ackermann H, Lutzenberger W, Dichgans J, Birbaumer N. 1993. Classical conditioning after cerebellar lesions in humans. Behav Neurosci 107:748–756.PubMedCrossRefGoogle Scholar
  18. 18.
    Dimitrova A, Weber J, Maschke M, Elles H-G, Kolb FP, Forsting M, Diener HC, Timmann D. 2002. Cerebellar and brainstem areas controlling human eyeblink responses as revealed by fMRI. Hum Brain Mapping 17:100–115.CrossRefGoogle Scholar
  19. 19.
    Drepper J, Timmann D, Kolb FP, Diener HC. 1999. Non-motor associative learning in patients with isolated degenerative cerebellar disease. Brain 122:87–97.PubMedCrossRefGoogle Scholar
  20. 20.
    Dudai Y. 2002. Memory from A to Z: Keywords, concepts and beyond. Oxford UP, Oxford.Google Scholar
  21. 21.
    Eccles JC, Ito M, Szentagothai J. 1967. The cerebellum as a neuronal machine. Springer, Berlin.Google Scholar
  22. 22.
    Gerwig M, Dimitrova A, Kolb FP, Maschke M, Brol B, Kunnel A, Böring D, Thilmann AF, Forsting M, Diener HC, Timmann D. 2003. Comparison of eyeblink conditioning in patients with superior and posterior inferior cerebellar lesions. Brain 126:71–94.PubMedCrossRefGoogle Scholar
  23. 23.
    Gomez-Beldarrain M, Garcia-Monco JC, Rubio B, Pascual-Leone A. 1998. Effect of focal cerebellar lesions on procedural learning in the serial reaction time task. Exp Brain Res 120:25–30.PubMedCrossRefGoogle Scholar
  24. 24.
    Gomi H, Kawato M. 1992. Adaptive feedback control models of the vestibulocerebellum and spinocerebellum. Biol Cybern 68:105–114.PubMedCrossRefGoogle Scholar
  25. 25.
    Gormezano I, Kehoe EJ. 1975. Classical conditioning: some methodological-conceptual issues. In Handbook of learning an cognitive processes, Vol. 2: Condition and behavior theory, pp. 143–179. Ed. WK Estes. Lawrence Erlbaum Associates Hillsdale, NJ.Google Scholar
  26. 26.
    Hansen PD, Woollacott MH, Debu B. 1988. Postural responses to changing task conditions. Exp Brain Res 73:627–636.PubMedCrossRefGoogle Scholar
  27. 27.
    Hebb DO. 1949. The organization of behaviour. John Wiley, New York.Google Scholar
  28. 28.
    Holst von E, Mittelstaedt H. 1950. Das Reafferenzprinzip. Naturwissenschaften 37:464–476.CrossRefGoogle Scholar
  29. 29.
    Houk JC, Singh SP, Fisher C, Barto AG. 1990. An adaptive sensorimotor network inspired by the anatomy and physiology of the cerebellum. In Neural networks for control, pp. 301–348. Ed. WT Miller, RS Sutton, PJ Werbos. MIT Press, Cambridge.Google Scholar
  30. 30.
    Ito M, Kano M. 1982. 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 33:253–258.PubMedCrossRefGoogle Scholar
  31. 31.
    Ito M. 1984. The cerebellum and neural control. Raven Press, New York.Google Scholar
  32. 32.
    Jansen J, Brodal A. 1940. Experimental studies on the intrinsic fibers of the cerebellum, II: the corticonuclear projection. J Comp Neurol 73:267–321.CrossRefGoogle Scholar
  33. 33.
    Kawato M, Furukawa K, Suzuki R. 1987. A hierarchical neural-network model for control and learning of voluntary movement. Biol Cybern 57:169–185.PubMedCrossRefGoogle Scholar
  34. 34.
    Kawato M, Gomi H. 1992. A computational model of four regions of the cerebellum based on feedback-error learning. Biol Cybern 68:95–103.PubMedCrossRefGoogle Scholar
  35. 35.
    Kawato M. 1996. Learning internal models of the motor apparatus. In The acquisition of motor behavior in vertebrates, pp. 408–430. Ed. JR Bloedel, TJ Ebener, SP Wise. MIT Press, Cambridge.Google Scholar
  36. 36.
    Keshner EA, Allum JH, Pfaltz CR. 1987. Postural coactivation and adaptation in the sway stabilizing responses of normals and patients with bilateral vestibular deficit. Exp Brain Res 69:77–92.PubMedCrossRefGoogle Scholar
  37. 37.
    Kolb FP. 1983. Results from a simulation model describing a biological, sensory feedback information system. Informatik-Fachberichte 71:588–594.Google Scholar
  38. 38.
    Kolb FP, Rubia FJ. 1980. Information about peripheral events conveyed to the cerebellum via the climbing fiber system in the decerebrate cat. Exp Brain Res 38:363–373.PubMedCrossRefGoogle Scholar
  39. 39.
    Kolb FP, Rubia FJ, Bauswein E. 1987. Cerebellar unit responses of the mossy fibre system to passive movements in the decerebrate cat. Exp Brain Res 68:234–248.PubMedGoogle Scholar
  40. 40.
    Kolb FP, Irwin KB, Bloedel JR, Bracha V. 1997. Conditioned and unconditioned forelimb reflex systems in the cat: involvement of the intermediate cerebellum. Exp Brain Res 114:255–270.PubMedCrossRefGoogle Scholar
  41. 41.
    Kolb FP, Timmann D, Baier PC, Diener HC. 2000. Classically conditioned withdrawal reflex in cerebellar patients, 2: impaired unconditioned responses. Exp Brain Res 130:471–485.PubMedCrossRefGoogle Scholar
  42. 42.
    Kolb FP, Lachauer S, Maschke M, Timmann D. 2002. Classical conditioning of postural reflexes. Pflugers Arch 445:224–237.PubMedCrossRefGoogle Scholar
  43. 43.
    Kolb FP, Lachauer S, Maschke M, Timmann D. 2004. Classical conditioning of postural reflex in cerebellar patients. Exp Brain Res 159:163–179.Google Scholar
  44. 44.
    Larsell O. 1947. The development of the cerebellum in man in relation to its comparative anatomy. J Comp Neurol 87:85–129.CrossRefGoogle Scholar
  45. 45.
    Leaton, RN, Supple Jr WF. 1986. Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science 232:513–515.PubMedCrossRefGoogle Scholar
  46. 46.
    Leaton RN, Supple Jr WF. 1991. Medial cerebellum and long-term habituation of acoustic startle in rats. Behav Neurosci 105:804–816.PubMedCrossRefGoogle Scholar
  47. 47.
    Lopiano L, de’Sperati C, & Montarolo, P.G. 1990. Long-term habituation of the acoustic startle response: role of the cerebellar vermis. Neuroscience 35:79–84.PubMedCrossRefGoogle Scholar
  48. 48.
    Marr D. 1969. A theory of cerebellar cortex. J Physiol 202:437–470.PubMedGoogle Scholar
  49. 49.
    Maschke M, Drepper J, Kindsvater K, Kolb FP, Diener HC, Timmann D. 2000. Involvement of the human medial cerebellum in long-term habituation of the acoustic startle response. Exp Brain Res 133:359–367.PubMedCrossRefGoogle Scholar
  50. 50.
    Miller S, Oscarsson O. 1970. Termination and functional organization of spino-olivocerebellar paths. In The cerebellum in health and disease, pp. 172–200. Ed. WS Fields, WD Willis. Warren H. Green, St. Louis.Google Scholar
  51. 51.
    Molinari M, Leggio MG, Solida A, Ciorra R, Misciagna S, Silveri MC, Petrosini L. 1997. Cerebellum and procedural learning: evidence from focal cerebellar lesions. Brain 120:1753–1762.PubMedCrossRefGoogle Scholar
  52. 52.
    Nashner LM. 1976. Adapting reflexes controlling the human posture. Exp Brain Res 26:59–72.PubMedCrossRefGoogle Scholar
  53. 53.
    Nixon PD, Passingham RE. 1999. The cerebellum and cognition: cerebellar lesions do not impair spatial working memory or visual associative learning in monkeys. Eur J Neurosci 11:4070–4080.PubMedCrossRefGoogle Scholar
  54. 54.
    Nixon PD, Passingham RE. 2000. The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys. Neuropsychologia 38:1054–1072.PubMedCrossRefGoogle Scholar
  55. 55.
    Oscarsson O. 1980. Functional organization of olivary projection to the cerebellar anterior lobe. In The inferior olivary nucleus: anatomy and physiology, pp. 279–289. Ed. O Creutzfeldt, C de Montigny, Y Lamarra. Raven Press, New York.Google Scholar
  56. 56.
    Pellionisz A, Llinas R. 1979. Cerebellar coordination: covarant analysis and contravariant synthesis via metric tensor: a tensorial approach to the geometry of brain function. Neurosci Abs 5:342.Google Scholar
  57. 57.
    Pissiota A, Frans O, Fredrikson M, Langstrom B, Flaten MA. 2002. The human startle reflex and pons activation: a regional cerebral blood flow study. Eur J Neurosci 15:395–398.PubMedCrossRefGoogle Scholar
  58. 58.
    Ramnani N, Toni I, Josephs O, Ashburner J, Passingham RE. 2000. Learning-and expectation-related changes in the human brain during motor learning. J Neurophysiol 84:3026–35.PubMedGoogle Scholar
  59. 59.
    Robinson DA. 1976. Adaptive gain control of vestibuloocular reflex by the cerebellum. J Neurophysiol 35:954–969.Google Scholar
  60. 60.
    Rosenblatt F. 1958. The perceptron: a probabilistic model for information storage and organization in the brain. Psych Rev 65:386–408.CrossRefGoogle Scholar
  61. 61.
    Rushmer DS, Roberts WJ Augter GK. 1976. Climbing fiber responses of cerebellar Purkinje cells to passive movement of the cat forepaw. Brain Res 106:1–20.PubMedCrossRefGoogle Scholar
  62. 62.
    Schmahmann JD. 1997. The cerebellum and cognition. Academic Press, San Diego.Google Scholar
  63. 63.
    Schreurs BG, McIntosh AR, Bahro M, Herscovitch P, Sunderland T, Molchan SE. 1997. Lateralization and behavioral correlation of changes in regional cerebral blood flow with classical conditioning of the human eyeblink response. J Neurophysiol 77:2153–2163.PubMedGoogle Scholar
  64. 64.
    Schweighofer N, Arbib MA, Dominey PF. 1996a. A model of the cerebellum in adaptive control of saccadic gain, I: the model and its biological substrate. Biol Cybern 75:19–28.PubMedGoogle Scholar
  65. 65.
    Schweighofer N, Arbib MA, Dominey PF. 1996b. A model of the cerebellum in adaptive control of saccadic gain, II: simulation results. Biol Cybern 75:29–36.PubMedGoogle Scholar
  66. 66.
    Seidler RD, Purushotham A, Kim SG, Ugurbil K, Willingham D, Ashe J. 2002. Cerebellum activation associated with performance change but not motor learning. Science 296:2043–2046.PubMedCrossRefGoogle Scholar
  67. 67.
    Squire LR, Zola-Morgan S. 1991. The medial temporal lobe memory system. Science 253:1380–1386.PubMedCrossRefGoogle Scholar
  68. 68.
    Thach WT, Goodkin HP, Keating JG. 1992. The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci 15:403–442.PubMedCrossRefGoogle Scholar
  69. 69.
    Thach WT. 1998. What is the role of the cerebellum in motor learning and cognition? Trends Cogn Sci 2:331–337.CrossRefGoogle Scholar
  70. 70.
    Thompson RF, Kim JJ. 1996. Memory systems in the brain and localization of a memory. Proc Natl Acad Sci USA 93:13438–13444.PubMedCrossRefGoogle Scholar
  71. 71.
    Thompson RF, Bao S, Chen L, Cipriano BD, Grethe JS, Kim JJ, Thompson JK, Tracy JA, Weninger MS, Krupa DJ. 1997. Associative learning. Int Rev Neurobiol 41:151–189.PubMedGoogle Scholar
  72. 72.
    Timmann D, Musso C, Kolb FP, Rijntjes M, Jüptner M, Müller SP, Diener HC, Weiller C. 1998. Involvement of the human cerebellum during habituation of the acoustic startle response: a PET-study. J Neurol Neurosurg Psychiatry 65:771–773.PubMedCrossRefGoogle Scholar
  73. 73.
    Timmann D, Baier PC, Diener HC, Kolb FP. 2000. Classically conditioned withdrawal reflex in cerebellar patients, 1: impaired conditioned responses. Exp Brain Res 130:453–470.PubMedCrossRefGoogle Scholar
  74. 74.
    Timmann D, Drepper J, Maschke M, Kolb FP, Böring D, Thilmann AF, Diener HC. 2002. Motor deficits cannot explain impaired cognitive associative learning in cerebellar patients. Neuropsychologia 40:788–800.PubMedCrossRefGoogle Scholar
  75. 75.
    Topka H, Valls-Sole J, Massaquoi SG, Hallett M. 1993. Deficit in classical conditioning in patients with cerebellar degeneration. Brain 116:961–969.PubMedCrossRefGoogle Scholar
  76. 76.
    Tucker J, Harding AE, Jahanshahi M, Nixon PD, Rushworth M, Quinn NP, Thompson PD, Passingham RE. 1996. Associative learning in patients with cerebellar ataxia. Behav Neurosci 110:1229–1234.PubMedCrossRefGoogle Scholar
  77. 77.
    Voogd J, Glickstein M. 1998. The anatomy of the cerebellum. Trends Neurosci 21:370–375.PubMedCrossRefGoogle Scholar
  78. 78.
    Widrow B, Lehr MA. 1990. Thirty years of adaptive neural networks: perceptron, madaline, and backpropagation. Proc IEEE 78:1415–1442.CrossRefGoogle Scholar
  79. 79.
    Wolpert DM, Miall RC, Kawato M. 1998. Internal models in the cerebellum. Trends Cogn Sci 2:338–347.CrossRefGoogle Scholar
  80. 80.
    Woodruff-Pak DS, Papka M, Ivry RB. 1996. Cerebellar involvement in eyeblink classical conditioning in humans. Neuropsychology 10:443–458.CrossRefGoogle Scholar
  81. 81.
    Yeo CH, Hesslow G. 1998. Cerebellum and conditioned reflexes. Trends Cogn Sci 2:322–330.CrossRefGoogle Scholar

Copyright information

© Springer Inc. 2006

Authors and Affiliations

  1. 1.Institute of PhysiologyUniversity of MunichMunichGermany
  2. 2.Department of NeurologyUniversity of Duisburg-EssenEssenGermany

Personalised recommendations