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Diversity and dynamism in the cerebellum

A Publisher Correction to this article was published on 04 January 2021

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Abstract

The past several years have brought revelations and paradigm shifts in research on the cerebellum. Historically viewed as a simple sensorimotor controller with homogeneous architecture, the cerebellum is increasingly implicated in cognitive functions. It possesses an impressive diversity of molecular, cellular and circuit mechanisms, embedded in a dynamic, recurrent circuit architecture. Recent insights about the diversity and dynamism of the cerebellum provide a roadmap for the next decade of cerebellar research, challenging some old concepts, reinvigorating others and defining major new research directions.

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Fig. 1: Intricacies of the cerebellar circuit.
Fig. 2: Revision of canonical ideas about inputs to the cerebellum via mossy fiber and climbing fiber pathways, based on recent discoveries.
Fig. 3: A potential solution for learned timing: a temporal basis set plus highly selective and specialized temporal contingencies for plasticity.
Fig. 4: Possible transfer of learning from early acquisition in the cerebellar cortex to consolidation in the cerebellar nucleus.

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References

  1. Witter, L., Rudolph, S., Pressler, R. T., Lahlaf, S. I. & Regehr, W. G. Purkinje cell collaterals enable output signals from the cerebellar cortex to feed back to Purkinje cells and interneurons. Neuron 91, 312–319 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. Rieubland, S., Roth, A. & Häusser, M. Structured connectivity in cerebellar inhibitory networks. Neuron 81, 913–929 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  3. Arlt, C. & Häusser, M. Microcircuit rules governing impact of single interneurons on Purkinje cell output in vivo. Cell Rep. 30, 3020–3035.e3 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  4. Hull, C. & Regehr, W. G. Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity. Neuron 73, 149–158 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Mann-Metzer, P. & Yarom, Y. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons. J. Neurosci. 19, 3298–3306 (1999).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  6. Dugué, G. P. et al. Electrical coupling mediates tunable low-frequency oscillations and resonance in the cerebellar Golgi cell network. Neuron 61, 126–139 (2009).

    Article  PubMed  Google Scholar 

  7. Zampini, V. et al. Mechanisms and functional roles of glutamatergic synapse diversity in a cerebellar circuit. eLife 5, e15872 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  8. Guo, C. et al. Purkinje Cells directly inhibit granule cells in specialized regions of the cerebellar cortex. Neuron 91, 1330–1341 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  9. Houck, B. D. & Person, A. L. Cerebellar premotor output neurons collateralize to innervate the cerebellar cortex. J. Comp. Neurol. 523, 2254–2271 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Gao, Z. et al. Excitatory cerebellar nucleocortical circuit provides internal amplification during associative conditioning. Neuron 89, 645–657 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Vervaeke, K. et al. Rapid desynchronization of an electrically coupled interneuron network with sparse excitatory synaptic input. Neuron 67, 435–451 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. van Welie, I., Roth, A., Ho, S. S. N., Komai, S. & Häusser, M. Conditional spike transmission mediated by electrical coupling ensures millisecond precision-correlated activity among interneurons in vivo. Neuron 90, 810–823 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Vervaeke, K., Lorincz, A., Nusser, Z. & Silver, R. A. Gap junctions compensate for sublinear dendritic integration in an inhibitory network. Science 335, 1624–1628 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Khilkevich, A., Zambrano, J., Richards, M.-M. & Mauk, M. D. Cerebellar implementation of movement sequences through feedback. Elife 7, e37443 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Voogd, J., Pardoe, J., Ruigrok, T. J. H. & Apps, R. The distribution of climbing and mossy fiber collateral branches from the copula pyramidis and the paramedian lobule: congruence of climbing fiber cortical zones and the pattern of zebrin banding within the rat cerebellum. J. Neurosci. 23, 4645–4656 (2003).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  16. Sugihara, I. & Shinoda, Y. Molecular, topographic, and functional organization of the cerebellar cortex: a study with combined aldolase C and olivocerebellar labeling. J. Neurosci. 24, 8771–8785 (2004).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  17. Zhou, H. et al. Cerebellar modules operate at different frequencies. eLife 3, e02536 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  18. De Zeeuw, C. I. et al. Spatiotemporal firing patterns in the cerebellum. Nat. Rev. Neurosci. 12, 327–344 (2011).

    Article  PubMed  Google Scholar 

  19. Cerminara, N. L., Lang, E. J., Sillitoe, R. V. & Apps, R. Redefining the cerebellar cortex as an assembly of non-uniform Purkinje cell microcircuits. Nat. Rev. Neurosci. 16, 79–93 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Rodriques, S. G. et al. Slide-seq: a scalable technology for measuring genome-wide expression at high spatial resolution. Science 363, 1463–1467 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Fujita, H., Kodama, T. & du Lac, S. Modular output circuits of the fastigial nucleus for diverse motor and nonmotor functions of the cerebellar vermis. eLife 9, e58613 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Lee, S. K., Sillitoe, R. V., Silva, C., Martina, M. & Sekerkova, G. α-Synuclein expression in the mouse cerebellum is restricted to VGluT1 excitatory terminals and is enriched in unipolar brush cells. Cerebellum 14, 516–527 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Kozareva, V. et al. A transcriptomic atlas of the mouse cerebellum reveals regional specializations and novel cell types. Preprint at bioRxiv https://doi.org/10.1101/2020.03.04.976407 (2020).

  24. Marr, D. A theory of cerebellar cortex. J. Physiol. (Lond.) 202, 437–470 (1969).

    Article  PubMed  CAS  Google Scholar 

  25. Albus, J. S. A theory of cerebellar function. Math. Biosci. 10, 25–61 (1971).

    Article  Google Scholar 

  26. Ito, M. Neural design of the cerebellar motor control system. Brain Res. 40, 81–84 (1972).

    Article  PubMed  CAS  Google Scholar 

  27. 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. 33, 253–258 (1982).

    Article  PubMed  CAS  Google Scholar 

  28. Hansel, C., Linden, D. J. & D’Angelo, E. Beyond parallel fiber LTD: the diversity of synaptic and non-synaptic plasticity in the cerebellum. Nat. Neurosci. 4, 467–475 (2001).

    Article  PubMed  CAS  Google Scholar 

  29. Carey, M. R. Synaptic mechanisms of sensorimotor learning in the cerebellum. Curr. Opin. Neurobiol. 21, 609–615 (2011).

    Article  PubMed  CAS  Google Scholar 

  30. Gao, Z., van Beugen, B. J. & De Zeeuw, C. I. Distributed synergistic plasticity and cerebellar learning. Nat. Rev. Neurosci. 13, 619–635 (2012).

    Article  PubMed  CAS  Google Scholar 

  31. Jörntell, H., Bengtsson, F., Schonewille, M. & De Zeeuw, C. I. Cerebellar molecular layer interneurons - computational properties and roles in learning. Trends Neurosci. 33, 524–532 (2010).

    Article  PubMed  Google Scholar 

  32. Boele, H. J. et al. Impact of parallel fiber to Purkinje cell long-term depression is unmasked in absence of inhibitory input. Sci. Adv. 4, s9426 (2018).

    Article  Google Scholar 

  33. Brown, A. M. et al. Molecular layer interneurons shape the spike activity of cerebellar Purkinje cells. Sci. Rep. 9, 1742 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Rowan, M. J. M. et al. Graded control of climbing-fiber-mediated plasticity and learning by inhibition in the cerebellum. Neuron 99, 999–1015.e6 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Boyden, E. S. et al. Selective engagement of plasticity mechanisms for motor memory storage. Neuron 51, 823–834 (2006).

    Article  PubMed  CAS  Google Scholar 

  36. Kimpo, R. R., Rinaldi, J. M., Kim, C. K., Payne, H. L. & Raymond, J. L. Gating of neural error signals during motor learning. eLife 3, e02076 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mathy, A., Clark, B. A. & Häusser, M. Synaptically induced long-term modulation of electrical coupling in the inferior olive. Neuron 81, 1290–1296 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Ebner, T. J., Wang, X., Gao, W., Cramer, S. W. & Chen, G. Parasagittal zones in the cerebellar cortex differ in excitability, information processing, and synaptic plasticity. Cerebellum 11, 418–419 (2012).

    Article  PubMed  Google Scholar 

  39. Voges, K., Wu, B., Post, L., Schonewille, M. & De Zeeuw, C. I. Mechanisms underlying vestibulo-cerebellar motor learning in mice depend on movement direction. J. Physiol. (Lond.) 595, 5301–5326 (2017).

    Article  PubMed  CAS  Google Scholar 

  40. ten Brinke, M. M. et al. Evolving models of Pavlovian conditioning: cerebellar cortical dynamics in awake behaving mice. Cell Rep. 13, 1977–1988 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  41. Suvrathan, A., Payne, H. L. & Raymond, J. L. Timing rules for synaptic plasticity matched to behavioral function. Neuron 92, 959–967 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Heffley, W. et al. Coordinated cerebellar climbing fiber activity signals learned sensorimotor predictions. Nat. Neurosci. 21, 1431–1441 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Heffley, W. & Hull, C. Classical conditioning drives learned reward prediction signals in climbing fibers across the lateral cerebellum. eLife 8, e46764 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kostadinov, D., Beau, M., Blanco-Pozo, M. & Häusser, M. Predictive and reactive reward signals conveyed by climbing fiber inputs to cerebellar Purkinje cells. Nat. Neurosci. 22, 950–962 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Larry, N., Yarkoni, M., Lixenberg, A. & Joshua, M. Cerebellar climbing fibers encode expected reward size. eLife 8, e46870 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Wagner, M. J., Kim, T. H., Savall, J., Schnitzer, M. J. & Luo, L. Cerebellar granule cells encode the expectation of reward. Nature 544, 96–100 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  47. Wagner, M. J. et al. Shared cortex-cerebellum dynamics in the execution and learning of a motor task. Cell 177, 669–682.e24 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  48. Sendhilnathan, N., Semework, M., Goldberg, M. E. & Ipata, A. E. Neural correlates of reinforcement learning in mid-lateral cerebellum. Neuron 106, 188–198.e5 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  49. Albergaria, C., Silva, N. T., Pritchett, D. L. & Carey, M. R. Locomotor activity modulates associative learning in mouse cerebellum. Nat. Neurosci. 21, 725–735 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  50. Bostan, A. C. & Strick, P. L. The basal ganglia and the cerebellum: nodes in an integrated network. Nat. Rev. Neurosci. 19, 338–350 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Carta, I., Chen, C. H., Schott, A. L., Dorizan, S. & Khodakhah, K. Cerebellar modulation of the reward circuitry and social behavior. Science 363, eaav0581 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  52. De Zeeuw, C. I. et al. Microcircuitry and function of the inferior olive. Trends Neurosci. 21, 391–400 (1998).

    Article  PubMed  Google Scholar 

  53. Medina, J. F. & Lisberger, S. G. Links from complex spikes to local plasticity and motor learning in the cerebellum of awake-behaving monkeys. Nat. Neurosci. 11, 1185–1192 (2008).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  54. Yang, Y. & Lisberger, S. G. Purkinje-cell plasticity and cerebellar motor learning are graded by complex-spike duration. Nature 510, 529–532 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Herzfeld, D. J., Hall, N. J., Tringides, M. & Lisberger, S. G. Principles of operation of a cerebellar learning circuit. eLife 9, e55217 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Braitenberg, V. Is the cerebellar cortex a biological clock in the millisecond range? Prog. Brain Res. 25, 334–346 (1967).

    Article  PubMed  CAS  Google Scholar 

  57. Payne, H. L. et al. Cerebellar Purkinje cells control eye movements with a rapid rate code that is invariant to spike irregularity. eLife 8, e37102 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Mauk, M. D. & Ruiz, B. P. Learning-dependent timing of Pavlovian eyelid responses: differential conditioning using multiple interstimulus intervals. Behav. Neurosci. 106, 666–681 (1992).

    Article  PubMed  CAS  Google Scholar 

  59. Perrett, S. P., Ruiz, B. P. & Mauk, M. D. Cerebellar cortex lesions disrupt learning-dependent timing of conditioned eyelid responses. J. Neurosci. 13, 1708–1718 (1993).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. Koekkoek, S. K. et al. Cerebellar LTD and learning-dependent timing of conditioned eyelid responses. Science 301, 1736–1739 (2003).

    Article  PubMed  CAS  Google Scholar 

  61. Ivry, R. B., Keele, S. W. & Diener, H. C. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp. Brain Res. 73, 167–180 (1988).

    Article  PubMed  CAS  Google Scholar 

  62. Spencer, R. M., Verstynen, T., Brett, M. & Ivry, R. Cerebellar activation during discrete and not continuous timed movements: an fMRI study. Neuroimage 36, 378–387 (2007).

    Article  PubMed  Google Scholar 

  63. Onuki, Y., Van Someren, E. J. W., De Zeeuw, C. I. & Van der Werf, Y. D. Hippocampal-cerebellar interaction during spatio-temporal prediction. Cereb. Cortex 25, 313–321 (2015).

    Article  PubMed  Google Scholar 

  64. Chabrol, F. P., Blot, A. & Mrsic-Flogel, T. D. Cerebellar contribution to preparatory activity in motor neocortex. Neuron 103, 506–519.e4 (2019).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. Gao, Z. et al. A cortico-cerebellar loop for motor planning. Nature 563, 113–116 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Buonomano, D. V. & Mauk, M. D. Neural network model of the cerebellum: temporal discrimination and timing of motor responses. Neural Comput. 6, 38–55 (1994).

    Article  Google Scholar 

  67. Chabrol, F. P., Arenz, A., Wiechert, M. T., Margrie, T. W. & DiGregorio, D. A. Synaptic diversity enables temporal coding of coincident multisensory inputs in single neurons. Nat. Neurosci. 18, 718–727 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Johansson, F., Jirenhed, D. A., Rasmussen, A., Zucca, R. & Hesslow, G. Memory trace and timing mechanism localized to cerebellar Purkinje cells. Proc. Natl. Acad. Sci. USA 111, 14930–14934 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Kennedy, A. et al. A temporal basis for predicting the sensory consequences of motor commands in an electric fish. Nat. Neurosci. 17, 416–422 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Giovannucci, A. et al. Cerebellar granule cells acquire a widespread predictive feedback signal during motor learning. Nat. Neurosci. 20, 727–734 (2017).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  71. Knogler, L. D., Markov, D. A., Dragomir, E. I., Štih, V. & Portugues, R. Sensorimotor representations in cerebellar granule cells in larval zebrafish are dense, spatially organized, and non-temporally patterned. Curr. Biol. 27, 1288–1302 (2017).

    Article  PubMed  CAS  Google Scholar 

  72. Sylvester, S. J. G. et al. Population-scale organization of cerebellar granule neuron signaling during a visuomotor behavior. Sci. Rep. 7, 16240 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  73. Sutton, R. S. & Barto, A. G. Toward a modern theory of adaptive networks: expectation and prediction. Psychol. Rev. 88, 135–170 (1981).

    Article  PubMed  CAS  Google Scholar 

  74. Ohyama, T., Nores, W. L. & Mauk, M. D. Stimulus generalization of conditioned eyelid responses produced without cerebellar cortex: implications for plasticity in the cerebellar nuclei. Learn. Mem. 10, 346–354 (2003).

    Article  PubMed  PubMed Central  Google Scholar 

  75. Kassardjian, C. D. et al. The site of a motor memory shifts with consolidation. J. Neurosci. 25, 7979–7985 (2005).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  76. Shutoh, F., Ohki, M., Kitazawa, H., Itohara, S. & Nagao, S. Memory trace of motor learning shifts transsynaptically from cerebellar cortex to nuclei for consolidation. Neuroscience 139, 767–777 (2006).

    Article  PubMed  CAS  Google Scholar 

  77. Nagao, S., Honda, T. & Yamazaki, T. Transfer of memory trace of cerebellum-dependent motor learning in human prism adaptation: a model study. Neural Netw. 47, 72–80 (2013).

    Article  PubMed  Google Scholar 

  78. Yamazaki, T., Nagao, S., Lennon, W. & Tanaka, S. Modeling memory consolidation during posttraining periods in cerebellovestibular learning. Proc. Natl. Acad. Sci. USA 112, 3541–3546 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Jang, D. C., Shim, H. G. & Kim, S. J. Intrinsic plasticity of cerebellar Purkinje cells contributes to motor memory consolidation. J. Neurosci. 40, 4145–4157 (2020).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  80. Ohmae, S. & Medina, J. F. Climbing fibers encode a temporal-difference prediction error during cerebellar learning in mice. Nat. Neurosci. 18, 1798–1803 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  81. Yang, Y. & Lisberger, S. G. Interaction of plasticity and circuit organization during the acquisition of cerebellum-dependent motor learning. eLife 2, e01574 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  82. Herzfeld, D. J., Kojima, Y., Soetedjo, R. & Shadmehr, R. Encoding of error and learning to correct that error by the Purkinje cells of the cerebellum. Nat. Neurosci. 21, 736–743 (2018).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Badura, A. et al. Climbing fiber input shapes reciprocity of Purkinje cell firing. Neuron 78, 700–713 (2013).

    Article  PubMed  CAS  Google Scholar 

  84. Miles, F. A. & Lisberger, S. G. Plasticity in the vestibulo-ocular reflex: a new hypothesis. Annu. Rev. Neurosci. 4, 273–299 (1981).

    Article  PubMed  CAS  Google Scholar 

  85. Lisberger, S. G. Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. J. Neurophysiol. 72, 974–998 (1994).

    Article  PubMed  CAS  Google Scholar 

  86. Carcaud, J. et al. Long-lasting visuo-vestibular mismatch in freely-behaving mice reduces the vestibulo-ocular reflex and leads to neural changes in the direct vestibular pathway. eNeuro 4, ENEURO.0290–16.2017 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  87. Nguyen-Vu, T. D. et al. Cerebellar Purkinje cell activity drives motor learning. Nat. Neurosci. 16, 1734–1736 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Attwell, P. J., Cooke, S. F. & Yeo, C. H. Cerebellar function in consolidation of a motor memory. Neuron 34, 1011–1020 (2002).

    Article  PubMed  CAS  Google Scholar 

  89. Okamoto, T., Shirao, T., Shutoh, F., Suzuki, T. & Nagao, S. Post-training cerebellar cortical activity plays an important role for consolidation of memory of cerebellum-dependent motor learning. Neurosci. Lett. 504, 53–56 (2011).

    Article  PubMed  CAS  Google Scholar 

  90. Fredette, B. J. & Mugnaini, E. The GABAergic cerebello-olivary projection in the rat. Anat. Embryol. (Berl.) 184, 225–243 (1991).

    Article  PubMed  CAS  Google Scholar 

  91. Lang, E. J., Sugihara, I. & Llinás, R. GABAergic modulation of complex spike activity by the cerebellar nucleoolivary pathway in rat. J. Neurophysiol. 76, 255–275 (1996).

    Article  PubMed  CAS  Google Scholar 

  92. Bazzigaluppi, P., Ruigrok, T., Saisan, P., De Zeeuw, C. I. & de Jeu, M. Properties of the nucleo-olivary pathway: an in vivo whole-cell patch clamp study. PLoS One 7, e46360 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  93. Mathy, A. et al. Encoding of oscillations by axonal bursts in inferior olive neurons. Neuron 62, 388–399 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  94. Najafi, F. & Medina, J. F. Beyond “all-or-nothing” climbing fibers: graded representation of teaching signals in Purkinje cells. Front. Neural Circuits 7, 115 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  95. Ruigrok, T. J. & Voogd, J. Organization of projections from the inferior olive to the cerebellar nuclei in the rat. J. Comp. Neurol. 426, 209–228 (2000).

    Article  PubMed  CAS  Google Scholar 

  96. Apps, R. et al. Cerebellar modules and their role as operational cerebellar processing units: a consensus paper. Cerebellum 17, 654–682 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  97. Chaumont, J. et al. Clusters of cerebellar Purkinje cells control their afferent climbing fiber discharge. Proc. Natl. Acad. Sci. USA 110, 16223–16228 (2013).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  98. Medina, J. F., Nores, W. L. & Mauk, M. D. Inhibition of climbing fibres is a signal for the extinction of conditioned eyelid responses. Nature 416, 330–333 (2002).

    Article  PubMed  CAS  Google Scholar 

  99. Yang, Y. & Lisberger, S. G. Modulation of complex-spike duration and probability during cerebellar motor learning in visually guided smooth-pursuit eye movements of monkeys. eNeuro 4, 0115–0117 (2017).

    Article  Google Scholar 

  100. Rasmussen, A., Jirenhed, D. A., Wetmore, D. Z. & Hesslow, G. Changes in complex spike activity during classical conditioning. Front. Neural Circuits 8, 90 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

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C.I.D.Z., S.G.L. and J.L.R. contributed equally to the conceptualization and writing.

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Correspondence to Stephen G. Lisberger.

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De Zeeuw, C.I., Lisberger, S.G. & Raymond, J.L. Diversity and dynamism in the cerebellum. Nat Neurosci 24, 160–167 (2021). https://doi.org/10.1038/s41593-020-00754-9

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