Skip to main content
Log in

Cerebellar Synaptic Plasticity and the Credit Assignment Problem

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

Abstract

The mechanism by which a learnt synaptic weight change can contribute to learning or adaptation of brain function is a type of credit assignment problem, which is a key issue for many parts of the brain. In the cerebellum, detailed knowledge not only of the local circuitry connectivity but also of the topography of different sources of afferent/external information makes this problem particularly tractable. In addition, multiple forms of synaptic plasticity and their general rules of induction have been identified. In this review, we will discuss the possible roles of synaptic and cellular plasticity at specific locations in contributing to behavioral changes. Focus will be on the parts of the cerebellum that are devoted to limb control, which constitute a large proportion of the cortex and where the knowledge of the external connectivity is particularly well known. From this perspective, a number of sites of synaptic plasticity appear to primarily have the function of balancing the overall level of activity in the cerebellar circuitry, whereas the locations at which synaptic plasticity leads to functional changes in terms of limb control are more limited. Specifically, the postsynaptic forms of long-term potentiation (LTP) and long-term depression (LTD) at the parallel fiber synapses made on interneurons and Purkinje cells, respectively, are the types of plasticity that mediate the widest associative capacity and the tightest link between the synaptic change and the external functions that are to be controlled.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. van Kan PL, Gibson AR, Houk JC. Movement-related inputs to intermediate cerebellum of the monkey. J Neurophysiol. 1993;69(1):74–94.

    PubMed  Google Scholar 

  2. van Kan PL, Houk JC, Gibson AR. Output organization of intermediate cerebellum of the monkey. J Neurophysiol. 1993;69(1):57–73.

    PubMed  Google Scholar 

  3. Armstrong DM, Edgley SA. Discharges of Purkinje cells in the paravermal part of the cerebellar anterior lobe during locomotion in the cat. J Physiol. 1984;352:403–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Pasalar S et al. Force field effects on cerebellar Purkinje cell discharge with implications for internal models. Nat Neurosci. 2006;9(11):1404–11.

    Article  CAS  PubMed  Google Scholar 

  5. Spanne A et al. Spike generation estimated from stationary spike trains in a variety of neurons in vivo. Front Cell Neurosci. 2014;8:199.

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ito M, Sakurai M, Tongroach P. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol. 1982;324:113–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Ekerot CF, Kano M. Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res. 1985;342(2):357–60.

    Article  CAS  PubMed  Google Scholar 

  8. Jorntell H, Ekerot CF. Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons. Neuron. 2002;34(5):797–806.

    Article  CAS  PubMed  Google Scholar 

  9. Coesmans M et al. Bidirectional parallel fiber plasticity in the cerebellum under climbing fiber control. Neuron. 2004;44(4):691–700.

    Article  CAS  PubMed  Google Scholar 

  10. Lev-Ram V et al. A new form of cerebellar long-term potentiation is postsynaptic and depends on nitric oxide but not cAMP. Proc Natl Acad Sci U S A. 2002;99(12):8389–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Jorntell H, Ekerot CF. Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo. J Neurosci. 2003;23(29):9620–31.

    PubMed  Google Scholar 

  12. Rancillac A, Crepel F. Synapses between parallel fibres and stellate cells express long-term changes in synaptic efficacy in rat cerebellum. J Physiol. 2004;554(Pt 3):707–20.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Tanaka S et al. Long-term potentiation of inhibitory synaptic transmission onto cerebellar Purkinje neurons contributes to adaptation of vestibulo-ocular reflex. J Neurosci. 2013;33(43):17209–20.

    Article  CAS  PubMed  Google Scholar 

  14. Kano M, Fukunaga K, Konnerth A. Ca(2+)-induced rebound potentiation of gamma-aminobutyric acid-mediated currents requires activation of Ca2+/calmodulin-dependent kinase II. Proc Natl Acad Sci U S A. 1996;93(23):13351–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Ichise T et al. mGluR1 in cerebellar Purkinje cells essential for long-term depression, synapse elimination, and motor coordination. Science. 2000;288(5472):1832–5.

    Article  CAS  PubMed  Google Scholar 

  16. Weber JT et al. Long-term depression of climbing fiber-evoked calcium transients in Purkinje cell dendrites. Proc Natl Acad Sci U S A. 2003;100(5):2878–83.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Belmeguenai A et al. Intrinsic plasticity complements long-term potentiation in parallel fiber input gain control in cerebellar Purkinje cells. J Neurosci. 2010;30(41):13630–43.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Xu W, Edgley SA. Climbing fibre-dependent changes in Golgi cell responses to peripheral stimulation. J Physiol. 2008;586(Pt 20):4951–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mapelli J, D′Angelo E. The spatial organization of long-term synaptic plasticity at the input stage of cerebellum. J Neurosci. 2007;27(6):1285–96.

    Article  CAS  PubMed  Google Scholar 

  20. Leiras R et al. Processing afferent proprioceptive information at the main cuneate nucleus of anesthetized cats. J Neurosci. 2010;30(46):15383–99.

    Article  CAS  PubMed  Google Scholar 

  21. Ekerot CF, Larson B. Correlation between sagittal projection zones of climbing and mossy fibre paths in cat cerebellar anterior lobe. Brain Res. 1973;64:446–50.

    Article  CAS  PubMed  Google Scholar 

  22. Cooke JD et al. Organization of afferent connections to cuneocerebellar tract. Exp Brain Res. 1971;13(4):359–77.

    PubMed  Google Scholar 

  23. Cooke JD et al. Origin and termination of cuneocerebellar tract. Exp Brain Res. 1971;13(4):339–58.

    CAS  PubMed  Google Scholar 

  24. Edin B. Cutaneous afferents provide information about knee joint movements in humans. J Physiol. 2001;531(Pt 1):289–97.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Edin BB. Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin. J Neurophysiol. 1992;67(5):1105–13.

    CAS  PubMed  Google Scholar 

  26. Jorntell H, Ekerot CF. Properties of somatosensory synaptic integration in cerebellar granule cells in vivo. J Neurosci. 2006;26(45):11786–97.

    Article  PubMed  Google Scholar 

  27. Garwicz M, Jorntell H, Ekerot CF. Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone. J Physiol. 1998;512(Pt 1):277–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Spanne A, Jorntell H. Processing of multi-dimensional sensorimotor information in the spinal and cerebellar neuronal circuitry: a new hypothesis. PLoS Comput Biol. 2013;9(3):e1002979.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Oscarsson O. Functional organization of spinocerebellar paths, in Handbook of Sensory Physiology. In: Iggo A, editor. New York: Springer-Verlag; 1973. p. 339–380.

  30. Illert M, Lundberg A, Tanaka R. Integration in descending motor pathways controlling the forelimb in the cat. 2. Convergence on neurones mediating disynaptic cortico-motoneuronal excitation. Exp Brain Res. 1976;26(5):521–40.

    CAS  PubMed  Google Scholar 

  31. Jankowska E, Nilsson E, Hammar I. Processing information related to centrally initiated locomotor and voluntary movements by feline spinocerebellar neurones. J Physiol. 2011;589(Pt 23):5709–25.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Illert M et al. Integration in descending motor pathways controlling the forelimb in the cat. 7. Effects from the reticular formation on C3-C4 propriospinal neurones. Exp Brain Res. 1981;42(3–4):269–81.

    CAS  PubMed  Google Scholar 

  33. Alstermark B, Isa T. Circuits for skilled reaching and grasping. Annu Rev Neurosci. 2012;35:559–78.

    Article  CAS  PubMed  Google Scholar 

  34. Santello M, Baud-Bovy G, Jorntell H. Neural bases of hand synergies. Front Comput Neurosci. 2013;7:23.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Brodal P, Walberg F. The pontine projection to the crebellar anterior lobe. An experimental study in the cat with retrograde transport of horseradish peroxidase. Exp Brain Res. 1977;29(2):233–48.

    Article  CAS  PubMed  Google Scholar 

  36. Lisberger SG, Fuchs AF. 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. 1978;41(3):764–77.

    CAS  PubMed  Google Scholar 

  37. Noda H, Suzuki DA. Processing of eye movement signals in the flocculus of the monkey. J Physiol. 1979;294:349–64.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Escudero M, Cheron G, Godaux E. Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. II. Prepositus hypoglossal nucleus. J Neurophysiol. 1996;76(3):1775–85.

    CAS  PubMed  Google Scholar 

  39. Cheron G et al. Existence in the nucleus incertus of the cat of horizontal-eye-movement-related neurons projecting to the cerebellar flocculus. J Neurophysiol. 1995;74(3):1367–72.

    CAS  PubMed  Google Scholar 

  40. Prsa M et al. Characteristics of responses of Golgi cells and mossy fibers to eye saccades and saccadic adaptation recorded from the posterior vermis of the cerebellum. J Neurosci. 2009;29(1):250–62.

    Article  CAS  PubMed  Google Scholar 

  41. Jorntell H et al. Segregation of tactile input features in neurons of the cuneate nucleus. Neuron. 2014;83(6):1444–52.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Bengtsson F, Jorntell H. Sensory transmission in cerebellar granule cells relies on similarly coded mossy fiber inputs. Proc Natl Acad Sci U S A. 2009;106(7):2389–94.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Huang CC et al. Convergence of pontine and proprioceptive streams onto multimodal cerebellar granule cells. Elife. 2013;2:e00400.

    PubMed  PubMed Central  Google Scholar 

  44. Marr D. A theory of cerebellar cortex. J Physiol. 1969;202(2):437–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  46. Geborek P et al. Cerebellar cortical neuron responses evoked from the spinal border cell tract. Front Neural Circ. 2013;7:157.

    Google Scholar 

  47. Ekerot CF, Jorntell H. Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific. Eur J Neurosci. 2001;13(7):1303–10.

    Article  CAS  PubMed  Google Scholar 

  48. Geborek P, Bengtsson F, Jorntell H. Properties of bilateral spinocerebellar activation of cerebellar cortical neurons. Front Neural Circ. 2014;8:128–37.

    Google Scholar 

  49. Roggeri L et al. Tactile stimulation evokes long-term synaptic plasticity in the granular layer of cerebellum. J Neurosci. 2008;28(25):6354–9.

    Article  CAS  PubMed  Google Scholar 

  50. Gebre SA, Reeber SL, Sillitoe RV. Parasagittal compartmentation of cerebellar mossy fibers as revealed by the patterned expression of vesicular glutamate transporters VGLUT1 and VGLUT2. Brain Struct Funct. 2012;217(2):165–80.

    Article  CAS  PubMed  Google Scholar 

  51. Tolbert DL, Alisky JM, Clark BR. Lower thoracic upper lumbar spinocerebellar projections in rats: a complex topography revealed in computer reconstructions of the unfolded anterior lobe. Neuroscience. 1993;55(3):755–74.

    Article  CAS  PubMed  Google Scholar 

  52. Holtzman T et al. Cerebellar Golgi cells in the rat receive multimodal convergent peripheral inputs via the lateral funiculus of the spinal cord. J Physiol. 2006;577(Pt 1):69–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Holtzman T et al. Multiple extra-synaptic spillover mechanisms regulate prolonged activity in cerebellar Golgi cell-granule cell loops. J Physiol. 2011;589(Pt 15):3837–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Brickley SG, Cull-Candy SG, Farrant M. Development of a tonic form of synaptic inhibition in rat cerebellar granule cells resulting from persistent activation of GABAA receptors. J Physiol. 1996;497(Pt 3):753–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Bengtsson F, Geborek P, Jorntell H. Cross-correlations between pairs of neurons in cerebellar cortex in vivo. Neural Netw. 2013;47:88–94.

    Article  PubMed  PubMed Central  Google Scholar 

  56. Duguid I et al. Tonic inhibition enhances fidelity of sensory information transmission in the cerebellar cortex. J Neurosci. 2012;32(32):11132–43.

    Article  CAS  PubMed  Google Scholar 

  57. Bengtsson F, Svensson P, Hesslow G. Feedback control of Purkinje cell activity by the cerebello-olivary pathway. Eur J Neurosci. 2004;20(11):2999–3005.

    Article  CAS  PubMed  Google Scholar 

  58. Chaumont J et al. Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc Natl Acad Sci U S A. 2013;110(40):16223–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Bengtsson F, Hesslow G. Cerebellar control of the inferior olive. Cerebellum. 2006;5(1):7–14.

    Article  CAS  PubMed  Google Scholar 

  60. Cheron G et al. BK channels control cerebellar Purkinje and Golgi cell rhythmicity in vivo. PLoS One. 2009;4(11):e7991.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Sausbier M et al. Cerebellar ataxia and Purkinje cell dysfunction caused by Ca2 + −activated K+ channel deficiency. Proc Natl Acad Sci U S A. 2004;101(25):9474–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fremont R et al. Abnormal high-frequency burst firing of cerebellar neurons in rapid-onset dystonia-parkinsonism. J Neurosci. 2014;34(35):11723–32.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Chen G et al. Low-frequency oscillations in the cerebellar cortex of the tottering mouse. J Neurophysiol. 2009;101(1):234–45.

    Article  PubMed  PubMed Central  Google Scholar 

  64. Hashimoto K, Kano M. Functional differentiation of multiple climbing fiber inputs during synapse elimination in the developing cerebellum. Neuron. 2003;38(5):785–96.

    Article  CAS  PubMed  Google Scholar 

  65. Hansel C, Linden DJ. Long-term depression of the cerebellar climbing fiber–Purkinje neuron synapse. Neuron. 2000;26(2):473–82.

    Article  CAS  PubMed  Google Scholar 

  66. Jorntell H, Hansel C. Synaptic memories upside down: bidirectional plasticity at cerebellar parallel fiber-Purkinje cell synapses. Neuron. 2006;52(2):227–38.

    Article  PubMed  Google Scholar 

  67. Mandolesi G et al. GluRdelta2 expression in the mature cerebellum of hotfoot mice promotes parallel fiber synaptogenesis and axonal competition. PLoS One. 2009;4(4):e5243.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Morando L et al. Role of glutamate delta −2 receptors in activity-dependent competition between heterologous afferent fibers. Proc Natl Acad Sci U S A. 2001;98(17):9954–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Bravin M et al. Control of spine formation by electrical activity in the adult rat cerebellum. Proc Natl Acad Sci U S A. 1999;96(4):1704–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ekerot CF, Jorntell H. Parallel fiber receptive fields: a key to understanding cerebellar operation and learning. Cerebellum. 2003;2(2):101–9.

    Article  PubMed  Google Scholar 

  71. Sultan F, Bower JM. Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis. J Comp Neurol. 1998;393(3):353–73.

    Article  CAS  PubMed  Google Scholar 

  72. Jorntell H et al. Cerebellar molecular layer interneurons—computational properties and roles in learning. Trends Neurosci. 2010;33(11):524–32.

    Article  PubMed  Google Scholar 

  73. Gao W et al. Cerebellar cortical molecular layer inhibition is organized in parasagittal zones. J Neurosci. 2006;26(32):8377–87.

    Article  CAS  PubMed  Google Scholar 

  74. Montarolo PG, Palestini M, Strata P. The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat. J Physiol. 1982;332:187–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Cerminara NL, Rawson JA. Evidence that climbing fibers control an intrinsic spike generator in cerebellar Purkinje cells. J Neurosci. 2004;24(19):4510–7.

    Article  CAS  PubMed  Google Scholar 

  76. Eccles JC, Ito M, Szentágothai J. The cerebellum as a neuronal machine. Berlin: Springer; 1967.

    Book  Google Scholar 

  77. Ito M. The cerebellum and neural control. New York: Raven; 1984.

    Google Scholar 

  78. Dean P et al. The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci. 2010;11(1):30–43.

    Article  CAS  PubMed  Google Scholar 

  79. Marquez-Ruiz J, Cheron G. Sensory stimulation-dependent plasticity in the cerebellar cortex of alert mice. PLoS One. 2012;7(4):e36184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Sakurai M. Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J Physiol. 1987;394:463–80.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Jorntell H, Ekerot CF. Receptive field remodeling induced by skin stimulation in cerebellar neurons in vivo. Front Neural Circ. 2011;5:3.

    Google Scholar 

  82. Badura A et al. Climbing fiber input shapes reciprocity of Purkinje cell firing. Neuron. 2013;78(4):700–13.

    Article  CAS  PubMed  Google Scholar 

  83. Brooks JX, Cullen KE. The primate cerebellum selectively encodes unexpected self-motion. Curr Biol. 2013;23(11):947–55.

    Article  CAS  PubMed  Google Scholar 

  84. Dean P et al. An adaptive filter model of cerebellar zone C3 as a basis for safe limb control? J Physiol. 2013;591(Pt 22):5459–74.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Bengtsson F, Jorntell H. Specific relationship between excitatory inputs and climbing fiber receptive fields in deep cerebellar nuclear neurons. PLoS One. 2014;9(1):e84616.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Zhou H et al. Cerebellar modules operate at different frequencies. Elife. 2014;3:e02536.

    PubMed  PubMed Central  Google Scholar 

  87. Xiao J et al. Systematic regional variations in Purkinje cell spiking patterns. PLoS One. 2014;9(8):e105633.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Ekerot CF, Larson B. Termination in overlapping sagittal zones in cerebellar anterior lobe of mossy and climbing fiber paths activated from dorsal funiculus. Exp Brain Res. 1980;38(2):163–72.

    Article  CAS  PubMed  Google Scholar 

  89. Sillitoe RV et al. Golgi cell dendrites are restricted by Purkinje cell stripe boundaries in the adult mouse cerebellar cortex. J Neurosci. 2008;28(11):2820–6.

    Article  CAS  PubMed  Google Scholar 

  90. Chadderton P, Margrie TW, Hausser M. Integration of quanta in cerebellar granule cells during sensory processing. Nature. 2004;428(6985):856–60.

    Article  CAS  PubMed  Google Scholar 

Download references

Conflict of Interest

The author declares that he has no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Henrik Jörntell.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jörntell, H. Cerebellar Synaptic Plasticity and the Credit Assignment Problem. Cerebellum 15, 104–111 (2016). https://doi.org/10.1007/s12311-014-0623-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-014-0623-y

Keywords

Navigation