Influence of the Cerebellum in Anticipation and Mental Disorders

  • Pascal HilberEmail author


The cerebellum is involved in motor coordination and motor learning. Cerebellar plasticity can serve as a cellular basis of learning. Data obtained from humans and animals led to the supposition that this structure could be a comparator and play a crucial role in sensory anticipation and online sensorimotor control. Internal models aid in executing motion precisely and harmoniously with or without external sensory feedback. The analogy between control of body part motion and manipulation of mental representation suggests the cerebellum’s possible involvement in non-motor mental functions. Moreover cerebellar-lesioned or mutant animals exhibit cognitive and emotional disturbances, especially high reactivity to environmental changes, behavioral disinhibition, and stereotyped behavior. All these results and theoretical approaches support the idea that the cerebellum and its role in anticipation could represent an interesting field of investigation in the pathophysiology and the treatment of neuropsychiatric disorders such as autism.


Anticipation Cerebellum Internal models Psychiatric disorders 


  1. 1.
    Martin, G.B., Butz, G.B., Sigaud, O., Pezzulo, G.: Anticipations, brains, individual and social behavior: an introduction to anticipatory systems. In: Butz, M.V., Sigaud, O., Pezzulo, G., Baldassarre, G. (eds.) Anticipatory Behavior in Adaptive Learning Systems, pp. 1–18. Springer, Berlin (2007)Google Scholar
  2. 2.
    Fleischer, J.G.: Neural correlates of anticipation in Cerebellum, Basal Ganglia, and hippocampus. In: Butz, M.V., Sigaud, O., Pezzulo, G., Baldassarre, G. (eds.) Anticipatory behavior in adaptive learning systems, vol. 4520, pp. 19–34. Springer, Berlin (2007)CrossRefGoogle Scholar
  3. 3.
    Nadin, M.: Can predictive computation reach the level of anticipatory computing? Int. J. Appl. Res. Inf. Technol. Comput. 5(3), 171–200 (2014)CrossRefGoogle Scholar
  4. 4.
    Doya, K.: Complementary roles of basal ganglia and cerebellum in learning and motor control Kenji Doya. Curr. Opin. Neurobiol. 10, 732–739 (2000)CrossRefGoogle Scholar
  5. 5.
    Imamizu, H., Miyauchi, S., Tamada, T., Sasaki, Y., Takino, R., Pütz, B., Yoshioka, T., Kawato, M.: Human cerebellar activity reflecting an acquired internal model of a new tool. Nature 403(6766), 192–195 (2000)CrossRefGoogle Scholar
  6. 6.
    Bastian, A.J.: Learning to predict the future: the cerebellum adapts feedforward movement control. Curr. Opin. Neurobiol. 16(6), 645–649 (2006)CrossRefGoogle Scholar
  7. 7.
    Serrien, D.J., Wiesendanger, M.: Role of the cerebellum in tuning anticipatory and reactive grip force responses. J. Cogn. Neurosci. 11(6), 672–681 (1999)CrossRefGoogle Scholar
  8. 8.
    Thomas, A.: Le cervelet – Etude anatomique, clinique et physiologique. Steinheil, Paris (1897)Google Scholar
  9. 9.
    Binet, A., Thomas, A., Henri, V.: Le cervelet. Revue 4, 438–439 (1897)Google Scholar
  10. 10.
    Flourens, M. J. P.: Recherches expérimentales sur les propriétés et les fonctions du système nerveux dans les animaux vertébrés. Paris (1824)Google Scholar
  11. 11.
    Glickstein, M., Strata, P., Voogd, J.: Cerebellum: history. Neuroscience 162(3), 549–559 (2009)CrossRefGoogle Scholar
  12. 12.
    Schmahmann, J.D., Caplan, D.: Cognition, emotion and the cerebellum. Brain 129(pt. 2), 290–292 (2006)Google Scholar
  13. 13.
    Bürk, K.: Cognition in hereditary ataxia. Cerebellum 6(3), 280–286 (2007)CrossRefGoogle Scholar
  14. 14.
    Cooper, F.E., Grube, M., Elsegood, K.J., Welch, J.L., Kelly, T.P., Chinnery, P.F., Griffiths, T.D.: The contribution of the cerebellum to cognition in Spinocerebellar Ataxia Type 6. Behav. Neurol. 23(1–2), 3–15 (2010)CrossRefGoogle Scholar
  15. 15.
    Bürk, K., Globas, C., Bösch, S., Klockgether, T., Zühlke, C., Daum, I., Dichgans, J.: Cognitive deficits in spinocerebellar ataxia type 1, 2, and 3. J. Neurol. 250(2), 207–211 (2003)CrossRefGoogle Scholar
  16. 16.
    Valis, M., Masopust, J., Bažant, J., Ríhová, Z., Kalnická, D., Urban, A., Zumrová, A., Hort, J.: Cognitive changes in spinocerebellar ataxia type 2. Neuro Endocrinol. Lett. 32(3), 354–359 (2011)Google Scholar
  17. 17.
    Lilja, A., Hämäläinen, P., Kaitaranta, E., Rinne, R.: Cognitive impairment in spinocerebellar ataxia type 8. J. Neurol. Sci. 237(1–2), 31–38 (2005)CrossRefGoogle Scholar
  18. 18.
    Suenaga, M., Kawai, Y., Watanabe, H., Atsuta, N., Ito, M., Tanaka, F., Katsuno, M., Fukatsu, H., Naganawa, S., Sobue, G.: Cognitive impairment in spinocerebellar ataxia type 6. J. Neurol. Neurosurg. Psychiatry 79(5), 496–499 (2008)CrossRefGoogle Scholar
  19. 19.
    Garrard, P., Martin, N.H., Giunti, P., Cipolotti, L.: Cognitive and social cognitive functioning in spinocerebellar ataxia: a preliminary characterization. J. Neurol. 255(3), 398–405 (2008)CrossRefGoogle Scholar
  20. 20.
    Baillieux, H., De Smet, H.J., Dobbeleir, A., Paquier, P.F., De Deyn, P.P., Mariën, P.: Cognitive and affective disturbances following focal cerebellar damage in adults: a neuropsychological and SPECT study. Cortex 46(7), 869–879 (2009)CrossRefGoogle Scholar
  21. 21.
    Stoodley, C.J., Schmahmann, J.D.: The cerebellum and language: evidence from patients with cerebellar degeneration. Brain Lang. 110(3), 149–153 (2009)CrossRefGoogle Scholar
  22. 22.
    Zuchowski, M.L., Timmann, D., Gerwig, M.: Acquisition of conditioned eyeblink responses is modulated by cerebellar tDCS. Brain Stimul. 7(4), 525–531 (2014)CrossRefGoogle Scholar
  23. 23.
    Hoppenbrouwers, S.S., Schutter, D.J.L.G., Fitzgerald, P.B., Chen, R., Daskalakis, Z.J.: The role of the cerebellum in the pathophysiology and treatment of neuropsychiatric disorders: a review. Brain Res. Rev. 59(1), 185–200 (2008)CrossRefGoogle Scholar
  24. 24.
    Mohapatra, P.K., Misra, B.N., Patanaik, P., Sahoo, S.: Major depressive disorder—a co-morbid condition in a case of spino-cerebellar ataxia with writer’s cramp. Indian J. Psychiatry 45(4), 257 (2003)Google Scholar
  25. 25.
    Reyes, M., Gordon, A.: Cerebellar vermis in schizophrenia. Lancet 318(8248), 700–701 (1981)CrossRefGoogle Scholar
  26. 26.
    Perlov, E., Tebarzt van Elst, L., Buechert, M., Maier, S., Matthies, S., Ebert, D., Hesslinger, B., Philipsen, A.: H1-MR-spectroscopy of cerebellum in adult attention deficit/hyperactivity disorder. J. Psychiatr. Res. 44(14), 938–943 (2010)Google Scholar
  27. 27.
    Pujol, J., Soriano-Mas, C., Alonso, P., Cardoner, N., Menchón, J.M., Deus, J., Vallejo, J.: Mapping structural brain alterations in obsessive-compulsive disorder. Arch. Gen. Psychiatry 61, 720–730 (2004)CrossRefGoogle Scholar
  28. 28.
    Sun, Y., Lee, J., Kirby, R.: Brain imaging findings in dyslexia. Pediatr. Neonatol. 51(2), 89–96 (2010)CrossRefGoogle Scholar
  29. 29.
    Laycock, S.K., Wilkinson, I.D., Wallis, L.I., Darwent, G., Wonders, S.H., Fawcett, A.J., Griffiths, P.D., Nicolson, R.I.: Cerebellar volume and cerebellar metabolic characteristics in adults with dyslexia. Ann. N. Y. Acad. Sci. 236, 222–236 (2008)CrossRefGoogle Scholar
  30. 30.
    Allen, G.: Cerebellar contributions to autism spectrum disorders. Clin. Neurosci. Res. 6(3–4), 195–207 (2006)CrossRefGoogle Scholar
  31. 31.
    Schmahmann, J. D., Sherman, J. C.: The cerebellar cognitive affective syndrome. Brain 561–579 (1998)Google Scholar
  32. 32.
    Schmahmann, J.D.: Disorders of the cerebellum. J. Neuropsychiatr. 16(3), 367–378 (2004)CrossRefGoogle Scholar
  33. 33.
    Schmahmann, J.D.: Cognition, emotion and the cerebellum. Brain 129(pt. 2), 190–192 (2006)Google Scholar
  34. 34.
    Topka, H., Massaquoi, S.G., Benda, N., Hallett, M.: Motor skill learning in patients with cerebellar degeneration. J. Neurol. Sci. 158, 164–172 (1998)CrossRefGoogle Scholar
  35. 35.
    Lorivel, P. H. T.: Animal models of cognitive and emotional functions of the cerebellum. In: Pombano, L. J., Evans, D. M. (eds.) Cerebellum anatomy, functions and disorders, pp. 31–58. Nova Publishers (2012)Google Scholar
  36. 36.
    Markvartová, V., Cendelín, J., Vozeh, F.: Changes of motor abilities during ontogenetic development in Lurcher mutant mice. Neuroscience 168(3), 646–651 (2010)CrossRefGoogle Scholar
  37. 37.
    Le Marec, N., Caston, J., Lalonde, R.: Impaired motor skills on static and mobile beams in lurcher mutant mice. Exp. Brain Res. 116(1), 131–138 (1997)CrossRefGoogle Scholar
  38. 38.
    Thifault, S., Girouard, N., Lalonde, R.: Climbing sensorimotor skills in Lurcher mutant mice. Brain Res. Bull. 41(6), 385–390 (1996)CrossRefGoogle Scholar
  39. 39.
    Porras-García, M.E., Ruiz, R., Pérez-Villegas, E.M., Armengol, J.Á.: Motor learning of mice lacking cerebellar Purkinje cells. Front. Neuroanat. 7, 1–8 (2013)CrossRefGoogle Scholar
  40. 40.
    Hilber, P., Caston, J.: Motor skills and motor learning in Lurcher mutant mice during aging. Neuroscience 102(3), 615–623 (2001)CrossRefGoogle Scholar
  41. 41.
    Lorivel, T., Hilber, P.: Motor effects of delta 9 THC in cerebellar Lurcher mutant mice. Behav. Brain Res. 181(2), 248–253 (2007)CrossRefGoogle Scholar
  42. 42.
    Lorivel, T., Hilber, P.: Effects of chlordiazepoxide on the emotional reactivity and motor capacities in the cerebellar Lurcher mutant mice. Behav. Brain Res. 173(1), 122–128 (2006)CrossRefGoogle Scholar
  43. 43.
    Cendelín, J., Korelusová, I., Vozeh, F.: The effect of repeated rotarod training on motor skills and spatial learning ability in Lurcher mutant mice. Behav. Brain Res. 189(1), 65–74 (2008)CrossRefGoogle Scholar
  44. 44.
    Hilber, P., Lalonde, R., Caston, J.: An unsteady platform test for measuring static equilibrium in mice. J. Neurosci. Methods 88(2), 201–205 (1999)CrossRefGoogle Scholar
  45. 45.
    Holschneider, D.P., Yang, J., Guo, Y., Maarek, J.I.: Reorganization of functional brain maps after exercise training: Importance of cerebellar—thalamic—cortical pathway. Brain Res. 1184, 96–107 (2007)CrossRefGoogle Scholar
  46. 46.
    Doyon, J., Benali, H.: Reorganization and plasticity in the adult brain during learning of motor skills. Curr. Opin. Neurobiol. 15(2), 161–167 (2005)CrossRefGoogle Scholar
  47. 47.
    Ito, M.: Bases and implications of learning in the cerebellum–adaptive control and internal model mechanism. Prog. Brain Res. 148, 95–109 (2005)CrossRefGoogle Scholar
  48. 48.
    Albus, J.S.: A model of computation and representation in the brain. Inf. Sci. (Ny) 180(9), 1519–1554 (2010)CrossRefGoogle Scholar
  49. 49.
    Doyon, J., Penhune, V., Ungerleider, L.G.: Distinct contribution of the cortico-striatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41(3), 252–262 (2003)CrossRefGoogle Scholar
  50. 50.
    Ito, M.: Control of mental activities by internal models in the cerebellum. Nat. Rev. Neurosci. 9(4), 304–313 (2008)CrossRefGoogle Scholar
  51. 51.
    Ivry, R.: Exploring the role of the cerebellum in sensory anticipation and timing: commentary on Tesche and Karhu. Hum. Brain Mapp. 9(3), 115–118 (2000)CrossRefGoogle Scholar
  52. 52.
    Nixon, P.D., Passingham, R.E.: Predicting sensory events the role of the cerebellum in motor learning. Exp. Brain Res. 138, 251–257 (2001)CrossRefGoogle Scholar
  53. 53.
    Ito, M.: Cerebellar circuitry as a neuronal machine. Prog. Neurobiol. 78(3–5), 272–303 (2006)CrossRefGoogle Scholar
  54. 54.
    Ohyama, T., Nores, W.L., Murphy, M., Mauk, M.D.: What the cerebellum computes. Trends Neurosci. 26(4), 222–227 (2003)CrossRefGoogle Scholar
  55. 55.
    Wolpert, D.M., Miall, R.C., Kawato, M.: Internal models in the cerebellum. Trends Cogn. Sci. 2(9), 338–347 (1998)CrossRefGoogle Scholar
  56. 56.
    Miall, R.C., Weir, D.J., Wolpert, D.M., Stein, J.F.: Is the cerebellum a smith predictor? J. Mot. Behav. 25(3), 203–216 (1993)CrossRefGoogle Scholar
  57. 57.
    Tuma, J., Kolinko, Y., Vozeh, F., Cendelin, J.: Mutation-related differences in exploratory, spatial, and depressive-like behavior in PCD and Lurcher cerebellar mutant mice. Front. Behav. Neurosci. 9(116), 1–19 (2015)Google Scholar
  58. 58.
    Hilber, J.C.P., Jouen, F., Delhaye-Bouchaud, N., Mariani, J.: Differential roles of the cerebellar cortex and deep cerebellar nuclei in learning and retention of a spatial task: Studies in intact and cerebellectomized Lurcher mutant mice. Behav. Genet. 28(4), 299–308 (1998)CrossRefGoogle Scholar
  59. 59.
    Gasbarri, A., Pompili, A., Pacitti, C., Cicirata, F.: Comparative effects of lesions of the ponto-cerebellar and olivo-cerebellar pathways on motor and spatial learning in the rat. Neuroscience 116, 1131–1140 (2003)CrossRefGoogle Scholar
  60. 60.
    Meignin, C., Hilber, P., Caston, J.: Influence of stimulation of the olivocerebellar pathway by harmaline on spatial learning in the rat. Brain Res. 824(2), 277–283 (1999)CrossRefGoogle Scholar
  61. 61.
    Garthe, A., Kempermann, G.: An old test for new neurons: refining the morris water maze to study the functional relevance of adult hippocampal neurogenesis. Front. Neurosci. 7, 1–11 (2013)CrossRefGoogle Scholar
  62. 62.
    D’Hooge, R., De Deyn, P.P.: Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev. 36(1), 60–90 (2001)CrossRefGoogle Scholar
  63. 63.
    Mandolesi, L., Giuseppa, M., Spirito, F., Federico, F., Petrosini, L.: Is the cerebellum involved in the visuo-locomotor associative learning? Behav. Brain Res. 184, 47–56 (2007)Google Scholar
  64. 64.
    Petrosini, L., Leggio, M. G., Molinari, M.: The cerebellum in the spatial problem solving: a co-star or a guest star? Prog. Neurobiol. 56(98), 191–210 (1998)Google Scholar
  65. 65.
    Lalonde, R., Lamarre, Y., Smith, A.M.: Does the mutant mouse lurcher have deficits in spatially oriented behaviours? Brain Res. 455(1), 24–30 (1988)CrossRefGoogle Scholar
  66. 66.
    Passot, J.B., Sheynikhovich, D., Duvelle, É., Arleo, A.: Contribution of cerebellar sensorimotor adaptation to hippocampal spatial memory. PLoS One 7(4), e32560 (2012)CrossRefGoogle Scholar
  67. 67.
    Gross, H., Heinze, A., Seiler, T., Stephan, V.: Generative character of perception: a neural architecture for sensorimotor anticipation. Neural Netw. 12, 1101–1129 (1999)CrossRefGoogle Scholar
  68. 68.
    Hilber, P., Lorivel, T., Delarue, C., Caston, J.: Stress and anxious-related behaviors in Lurcher mutant mice. Brain Res. 1003(1–2), 108–112 (2004)CrossRefGoogle Scholar
  69. 69.
    Lorivel, T., Roy, V., Hilber, P.: Fear-related behaviors in Lurcher mutant mice exposed to a predator. Genes. Brain. Behav. 13(8), 794–801 (2014)CrossRefGoogle Scholar
  70. 70.
    Zhu, L., Scelfo, B., Tempia, F., Sacchetti, B., Strata, P.: Membrane excitability and fear conditioning in cerebellar Purkinje cell. Neuroscience 140(3), 801–810 (2006)CrossRefGoogle Scholar
  71. 71.
    Sacchetti, B., Scelfo, B., Tempia, F., Strata, P.: Long-term synaptic changes induced in the cerebellar cortex by fear conditioning. Neuron 42(6), 973–982 (2004)CrossRefGoogle Scholar
  72. 72.
    Sacchetti, B., Scelfo, B., Strata, P.: Cerebellum and emotional behavior. NSC 162(3), 756–762 (2009)Google Scholar
  73. 73.
    Parvizi, J., Anderson, S.W., Martin, C.O., Damasio, H., Damasio, A.R.: Pathological laughter and crying: a link to the cerebellum. Brain 124(pt. 9), 1708–1709 (2001)CrossRefGoogle Scholar
  74. 74.
    Tillfors, M., Furmark, T., Marteinsdottir, I., Fredrikson, M.: Cerebral blood flow during anticipation of public speaking in social phobia: a PET study. Biol. Psychiatry 52(11), 1113–1119 (2002)CrossRefGoogle Scholar
  75. 75.
    Smith, K.A., Ploghaus, A., Cowen, P.J., Mccleery, J.M., Guy, M., Smith, S., Tracey, I., Matthews, P.M.: Cerebellar responses during anticipation of noxious stimuli in subjects recovered from depression: Functional magnetic resonance imaging study. Br. J. Psychiatry 181, 411–415 (2002)CrossRefGoogle Scholar
  76. 76.
    Moulton, E.A., Elman, I., Pendse, G., Schmahmann, J., Becerra, L., Borsook, D.: Aversion-related circuitry in the cerebellum: responses to noxious heat and unpleasant images. J. Neurosci. 31(10), 3795–3804 (2011)CrossRefGoogle Scholar
  77. 77.
    Durisko, C., Fiez, J.A.: Functional activation in the cerebellum during working memory and simple speech tasks. Cortex 46(7), 896–906 (2010)CrossRefGoogle Scholar
  78. 78.
    Balsters, J.H., Ramnani, N.: Symbolic representations of action in the human cerebellum. Neuroimage 43(2), 388–398 (2008)CrossRefGoogle Scholar
  79. 79.
    Balser, N., Lorey, B., Pilgramm, S., Naumann, T., Kindermann, S., Stark, R., Zentgraf, K., Williams, A.M., Munzert, J.: The influence of expertise on brain activation of the action observation network during anticipation of tennis and volleyball serves. Front. Hum. Neurosci. 8, 568 (2014)CrossRefGoogle Scholar
  80. 80.
    Lee, T.M.C., Liu, H., Hung, K.N., Pu, J., Ng, Y., Mak, A.K.Y., Gao, J., Chan, C.C.H.: The cerebellum’s involvement in the judgment of spatial orientation: a functional magnetic resonance imaging study. Neuropsychologia 43, 1870–1877 (2005)CrossRefGoogle Scholar
  81. 81.
    Beaton, A., Mariën, P.: Language, cognition and the cerebellum: grappling with an enigma. Cortex 46(7), 811–820 (2010)CrossRefGoogle Scholar
  82. 82.
    Schweizer, T.A., Alexander, M.P., Cusimano, M., Stuss, D.T.: Fast and efficient visuotemporal attention requires the cerebellum. Neuropsychologia 45, 3068–3074 (2007)CrossRefGoogle Scholar
  83. 83.
    Kim, Y.T., Seo, J.H., Song, H.J., Yoo, D.S., Lee, H.J., Lee, J., Lee, G., Kwon, E., Kim, J.G., Chang, Y.: Neural correlates related to action observation in expert archers. Behav. Brain Res. 223(2), 342–347 (2011)CrossRefGoogle Scholar
  84. 84.
    Becker, E.B.E., Stoodley, C.J.: Autism spectrum disorder and the cerebellum. Int. Rev. Neurobiol. 113, 1–34 (2013)CrossRefGoogle Scholar
  85. 85.
    Gliga, T., Jones, E.J.H., Bedford, R., Charman, T., Johnson, M.H.: From early markers to neuro-developmental mechanisms of autism. Dev. Rev. 34(3), 189–207 (2014)CrossRefGoogle Scholar
  86. 86.
    Goines, P., Haapanen, L., Boyce, R., Duncanson, P., Braunschweig, D., Delwiche, L., Hansen, R., Hertz-Picciotto, I., Ashwood, P., Van de Water, J.: Autoantibodies to cerebellum in children with autism associate with behavior. Brain Behav. Immun. 25(3), 514–523 (2011)CrossRefGoogle Scholar
  87. 87.
    Kern, J.K.: Purkinje cell vulnerability and autism: a possible etiological connection. Brain Dev. 25(6), 377–382 (2003)CrossRefGoogle Scholar
  88. 88.
    Schroeder, J.H., Desrocher, M., Bebko, J.M., Cappadocia, M.C.: Research in Autism Spectrum Disorders The neurobiology of autism: theoretical applications. Res. Autism Spectr. Disord. 4(4), 555–564 (2010)CrossRefGoogle Scholar
  89. 89.
    Allen, G.: The cerebellum in autism. Clin. Neuropsychiatry 2(6), 321–337 (2005)Google Scholar
  90. 90.
    Larson, J.C.G., Bastian, A.J., Donchin, O., Shadmehr, R., Mostofsky, S.H.: Acquisition of internal models of motor tasks in children with autism. Brain 131(pt. 11), 2894–2903 (2008)CrossRefGoogle Scholar
  91. 91.
    Stoit, A.M.B., van Schie, H.T., Riem, M., Meulenbroek, R.G.J., Newman-Norlund, R.D., Slaats-Willemse, D.I.E., Bekkering, H., Buitelaar, J.K.: Internal model deficits impair joint action in children and adolescents with autism spectrum disorders. Res. Autism Spectr. Disord. 5(4), 1526–1537 (2011)CrossRefGoogle Scholar
  92. 92.
    Haswell, C.C., Izawa, J., Dowell, L.R., Mostofsky, S.H., Shadmehr, R.: Representation of internal models of action in the autistic brain. Nat. Neurosci. 12(8), 970–972 (2009)CrossRefGoogle Scholar
  93. 93.
    Martin, L.A., Goldowitz, D., Mittleman, G.: Repetitive behavior and increased activity in mice with Purkinje cell loss: a model for understanding the role of cerebellar pathology in autism. Eur. J. Neurosci. 31(3), 544–555 (2010)CrossRefGoogle Scholar
  94. 94.
    Nadin. M.: Anticipation and the Brain. In: Nadin, M. (ed.): Anticipation and Medicine, pp. 135–162. Springer, Cham, CH. (2016)Google Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  1. 1.Laboratory of Psychology and Neurosciences of Cognition and AffectivityRouen Normandy UniversityMont Saint AignanFrance

Personalised recommendations