The Cerebellum

, 6:193 | Cite as

Cerebellar contributions to verbal working memory: beyond cognitive theory

  • Gal Ben-YehudahEmail author
  • Sara Guediche
  • Julie A. Fiez
Original Article


Neuropsychological findings together with recent advances in neuroanatomical and neuroimaging techniques have spurred the investigation of cerebellar contributions to cognition. One cognitive process that has been the focus of much research is working memory, in particular its verbal component. Influenced by Baddeley’s cognitive theory of working memory, cerebellar activation during verbal working memory tasks has been predominantly attributed to the cerebellum’s involvement in an articulatory rehearsal network. Recent neuroimaging and neuropsychological findings are inconsistent with a simple motor view of the cerebellum’s function in verbal working memory. The present article examines these findings and their implications for an articulatory rehearsal proposal of cerebellar function. Moving beyond cognitive theory, we propose two alternative explanations for cerebellar involvement in verbal working memory: Error-driven adjustment and internal timing. These general theories of cerebellar function have been successfully adapted from the motor literature to explain cognitive functions of the cerebellum. We argue that these theories may also provide a useful framework to understand the non-motor contributions of the cerebellum to verbal working memory.

Key words

Cerebellum working memory rehearsal error correction timing 


  1. 1.
    Holmes G. The cerebellum of man. Brain. 1939;62(Part l):1–30.CrossRefGoogle Scholar
  2. 2.
    Leiner HC, Leiner AL, Dow RS. Does the cerebellum contribute to mental skills? Behav Neurosci. 1986;100:443–54.PubMedCrossRefGoogle Scholar
  3. 3.
    Bracke-Tolkmitt R, Linden A, Canavan AGM, Rockstroh B, Scholz E, Wessel K, et al. The cerebellum contributes to mental skills. Behav Neurosci. 1989;103(2):442–6.CrossRefGoogle Scholar
  4. 4.
    Ivry RB, Keele SW. Timing functions of the cerebellum. J Cognit Neurosci. 1989;1:136–52.CrossRefGoogle Scholar
  5. 5.
    Petersen SE, Fox PT, Posner MI, Mintun M, Raichle ME. Positron emission tomographic studies of the processing of single words. J Cognit Neurosci. 1989;1(2):153–70.CrossRefGoogle Scholar
  6. 6.
    Fiez JA, Petersen SE, Cheney MK, Raichle ME. Impaired non-motor learning and error detection associated with cerebellar damage. A single case study. Brain. 1992;115 Pt 1:155–78.PubMedCrossRefGoogle Scholar
  7. 7.
    Desmond JE, Fiez JA. Neuroimaging studies of the cerebellum: Language, learning and memory. Trends Cognit Sci. 1998;2(9):355–8.CrossRefGoogle Scholar
  8. 8.
    Ivry RB, Fiez JA. Cerebellar contributions to cognition and imagery. In: Gazzaniga MS, editor. The new cognitive neuroscience. Cambridge, MA: MIT Press; 2000. pp 999–1011.Google Scholar
  9. 9.
    Baddeley AD. Working memory. New York, NY: Oxford University Press; 1986.Google Scholar
  10. 10.
    Just MA, Carpenter PA. A capacity theory of comprehension: Individual differences in working memory. Psychological Rev. 1992;99(1):122–49.CrossRefGoogle Scholar
  11. 11.
    Baddeley A. Working memory: Looking back and looking forward. Nat Rev Neurosci. 2003;4(10):829–39.PubMedCrossRefGoogle Scholar
  12. 12.
    Miyake A, Shah P, editors. Models of working memory: Mechanisms of active maintenance and executive control. New York: Cambridge University Press; 1999.Google Scholar
  13. 13.
    Miller GA. The magical number seven, plus of minus two: Some limits on our capacity for processing information. Psychological Rev. 1956;63:81–97.CrossRefGoogle Scholar
  14. 14.
    Luck SJ, Vogel EK. The capacity of visual working memory for features and conjunctions. Nature. 1997;390(6657): 279–81.PubMedCrossRefGoogle Scholar
  15. 15.
    Paulesu E, Frith CD, Frackowiak RS. The neural correlates of the verbal component of working memory. Nature. 1993;362(6418):342–5.PubMedCrossRefGoogle Scholar
  16. 16.
    Chein JM, Fissell K, Jacobs S, Fiez JA. Functional heterogeneity within Broca’s area during verbal working memory. Physiol Behav. 2002;77(4–5):635–9.PubMedCrossRefGoogle Scholar
  17. 17.
    Hautzel H, Mottaghy FM, Schmidt D, Zemb M, Shah NJ, Muller-Gartner HW, et al. Topographic segregation and convergence of verbal, object, shape and spatial working memory in humans. Neurosci Lett. 2002;323:156–60.PubMedCrossRefGoogle Scholar
  18. 18.
    Wager TD, Smith EE. Neuroimaging studies of working memory: a meta-analysis. Cognit, Affect Behav Neurosci. 2003;3:255–74.Google Scholar
  19. 19.
    Middleton FA, Strick P. Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994;266:458–61.PubMedCrossRefGoogle Scholar
  20. 20.
    Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 2001;21:700–12.PubMedGoogle Scholar
  21. 21.
    Kelly R, Strick P. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432–44.PubMedGoogle Scholar
  22. 22.
    Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, Salek-Haddadi A, et al. Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortexin vivo. Neuroimage. 2003;19(4):1349–60.PubMedCrossRefGoogle Scholar
  23. 23.
    Hugdahl K. Lateralization of cognitive processes in the brain. Acta Psychol (Amst). 2000;105(2–3):211–35.CrossRefGoogle Scholar
  24. 24.
    Silveri M, Di Betta A, Filippini V, Leggio M, Molinari M. Verbal short-term store-rehearsal system and the cerebellum: Evidence from a patient with a right cerebellar lesion. Brain. 1998;121:2175–87.PubMedCrossRefGoogle Scholar
  25. 25.
    Hokkanen LSK, Kauranen V, Roine RO, Salonen O, Kotila M. Subtle cognitive deficits after cerebellar infarcts. EurJNeurol. 2006;13:161–70.Google Scholar
  26. 26.
    Ravizza SM, McCormick CA, Schlerf J, Justus T, Ivry RB, Fiez JA. Cerebellar damage produces selective deficits in verbal working memory. Brain. 2006;129:306–20.PubMedCrossRefGoogle Scholar
  27. 27.
    Awh E, Jonides J, Smith EE, Schumacher EH, Koeppe RA, Katz S. Dissociation of storage and rehearsal in verbal working memory: Evidence from positron emission tomography. Psychological Sci. 1996;7(1):25–31.CrossRefGoogle Scholar
  28. 28.
    Chein JM, Fiez JA. Dissociation of verbal working memory system components using a delayed serial recall task. Cereb Cortex. 2001;11(11):1003–14.PubMedCrossRefGoogle Scholar
  29. 29.
    Desmond JE, Gabrieli JD, Wagner AD, Ginier BL, Glover GH. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J Neurosci. 1997;17(24):9675–85.PubMedGoogle Scholar
  30. 30.
    Fiez JA, Raife EA, Balota DA, Schwarz JP, Raichle ME, Petersen SE. A positron emission tomography study of the short-term maintenance of verbal information. J Neurosci. 1996;16(2):808–22.PubMedGoogle Scholar
  31. 31.
    Jonides J, Schumacher EH, Smith EE, Koeppe RA, Awh E, Reuter Lorenz PA, et al. The role of parietal cortex in verbal working memory. J Neurosci. 1998;18(13):5026–34.PubMedGoogle Scholar
  32. 32.
    Smith EE, Jonides J, Marshuetz C, Koeppe RA. Components of verbal working memory: Evidence from neuroimaging. Proc Natl Acad Sci USA. 1998;95(3):876–82.PubMedCrossRefGoogle Scholar
  33. 33.
    Chen SHA, Desmond JE. Cerebrocerebellar networks during articulatory rehearsal and verbal working memory tasks. NeuroImage. 2005;24:332–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Chen SHA, Desmond JE. Temporal dynamics of cerebrocerebellar network recruitment during a cognitive task. Neuropsychologia. 2005;43:1227–37.PubMedCrossRefGoogle Scholar
  35. 35.
    Baddeley AD, Thomson N, Buchanan M. Word length and the structure of short-term memory. J Verbal Learn Verbal Behav. 1975;14(6):575–89.CrossRefGoogle Scholar
  36. 36.
    Marr D. A theory of cerebellar cortex. J Physiol. 1969;202:437–70.PubMedGoogle Scholar
  37. 37.
    Albus JS. A theory of cerebellar function. Mathemat Biosci. 1971;10:25–61.CrossRefGoogle Scholar
  38. 38.
    Ivry RB. The representation of temporal information in perception and motor control. Curr Opin Neurobiol. 1996;6:851–7.PubMedCrossRefGoogle Scholar
  39. 39.
    Ackermann H, Mathiak K, Ivry RB. Temporal organization of ‘internal speech’ as a basis for cerebellar modulation of cognitive functions. Behav Cognit Neurosci Rev. 2004;3(1):14–22.CrossRefGoogle Scholar
  40. 40.
    Barlow JS. The cerebellum and adaptive control. Cambridge, UK: Cambridge University Press; 2002.Google Scholar
  41. 41.
    Ito M. Cerebellar circuitry as a neuronal machine. Prog Neurobiol. 2006;78:272–303.PubMedCrossRefGoogle Scholar
  42. 42.
    Ito M. Cerebellar learning in the vestibulo-ocular reflex. Trends Cognit Sci. 1998;2(9):313–21.CrossRefGoogle Scholar
  43. 43.
    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(5):1262–75.PubMedGoogle Scholar
  44. 44.
    Kitazawa S, Kimura T, Yin P. Cerebellar complex spikes encode both destinations and errors in arm movement. Nature. 1998;392:494–7.PubMedCrossRefGoogle Scholar
  45. 45.
    Diedrichsen J, Hashambhoy Y, Rane T, Shadmehr R. Neural correlates of reach errors. J Neurosci. 2005;25(43):9919–31.PubMedCrossRefGoogle Scholar
  46. 46.
    Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cognit Sci. 1998;2(9):338–46.CrossRefGoogle Scholar
  47. 47.
    Postma A. Detection of errors during speech production: A review of speech monitoring models. Cognition. 2000;77:97–131.PubMedCrossRefGoogle Scholar
  48. 48.
    Levelt WJM. Models of word production. Trends Cognit Sci. 1999;3(6):223–32.CrossRefGoogle Scholar
  49. 49.
    Guenther FH, Ghosh SS, Tourville JA. Neural modeling and imaging of the cortical interactions underlying syllable production. Brain Lang. 2006;96:280–301.PubMedCrossRefGoogle Scholar
  50. 50.
    Duffy JR. Motor speech disorders. St Louis, MO: Mosby Inc.; 1995.Google Scholar
  51. 51.
    Baddeley AD, Wilson B. Phonological coding and short-term memory in patients without speech. J Memory Lang. 1985;24(4):490–502.CrossRefGoogle Scholar
  52. 52.
    Bishop DV, Robson J. Unimpaired short-term memory and rhyme judgement in congenitally speechless individuals: Implications for the notion of ‘articulatory coding’. Quart J Experim Psychol: Human Experim Psychol. 1989;41(1-A):123–40.Google Scholar
  53. 53.
    Kirschen MP, Chen SHA, Schraedley-Desmond P, Desmond JE. Load- and practice-dependent increases in cerebero-cerebellar activation in verbal working memory: An fMRI study. Neuroimage. 2005;24:462–72.PubMedCrossRefGoogle Scholar
  54. 54.
    Justus T, Ravizza SM, Fiez JA, Ivry RB. Reduced phonological similarity effects in patients with damage to the cerebellum. Brain Lang. 2005;95:304–18.PubMedCrossRefGoogle Scholar
  55. 55.
    Conrad R. Acoustic confusion in immediate memory. Br J Psychol. 1964;55:75–84.Google Scholar
  56. 56.
    Hulme C, Roodenrys S, Schweickert R, Brown GD, Martin M, Stuart G. Word-frequency effects on short-term memory tasks: Evidence for a redintegration process in immediate serial recall. J Exp Psychol Learn Mem Cogn. 1997;23(5):1217–32.PubMedCrossRefGoogle Scholar
  57. 57.
    Gathercole SE, Pickering SJ, Hall M, Peaker SM. Dissociable lexical and phonological influences on serial recognition and serial recall. Quart J Experim Psychol: Human Experim Psychol. 2001;54a(1):1–30.CrossRefGoogle Scholar
  58. 58.
    Ben-Yehudah G, Fiez JA. Impact of cerebellar lesions on reading and verbal working memory. In: Cognitive Neuroscience Society annual meeting. New York, USA; 2005.Google Scholar
  59. 59.
    Booth JR, Wood L, Dong L, Houk JC, Bitan T. The role of the basal ganglia and cerebellum in language processing. Brain Res. 2007;1133(1):136–44.PubMedCrossRefGoogle Scholar
  60. 60.
    Ivry R. Cerebellar timing systems. In: Schmahmann J, editor. The cerebellum and cognition. San Diego, CA: Academic Press; 1997. pp 555–73.Google Scholar
  61. 61.
    Ivry RB, Spencer RMC. The neural representation of time. Curr Opin Neurobiol. 2004;14:225–32.PubMedCrossRefGoogle Scholar
  62. 62.
    Braitenberg V. Is the cerebellar cortex a biological clock in the millisecond range? Prog Brain Res. 1967;25:334–46.PubMedGoogle Scholar
  63. 63.
    Timmann D, Watts S, Höre J. Failure of cerebellar patients to time finger opening precisely causes ball high-low inaccuracy in overarm throws. J Neurophysiol. 1999;2: 103–14.Google Scholar
  64. 64.
    McNaughton S, Timmann D, Watts S, Hore J. Overarm throwing speed in cerebellar subjects: Effect of timing of ball release. Experim Brain Res. 2004;154:470–8.CrossRefGoogle Scholar
  65. 65.
    Ivry R, Keele S, Diener H. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Experim Brain Res. 1988;73(1):167–80.CrossRefGoogle Scholar
  66. 66.
    Levelt WJM. Speaking: From intention to articulation. Cambridge, MA: MIT Press; 1989.Google Scholar
  67. 67.
    Hertrich IA. Acoustic analysis of durational speech parameters in neurological dysarthrias. In: Lebrun Y, editor. From the brain to the mouth: Acquired dysarthria and dysfluency in adults. Dordrecht, The Netherlands: Kluwer; 1997. pp 11–47.Google Scholar
  68. 68.
    Ackermann H, Graber S, Hertrich I, Daum I. Categorical speech perception in cerebellar disorders. Brain Lang. 1997;60:323–31.PubMedCrossRefGoogle Scholar
  69. 69.
    Henson RN, Burgess N, Frith CD. Recoding, storage, rehearsal and grouping in verbal short-term memory: An fMRI study. Neuropsychologia. 2000;38(4):426–40.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Gal Ben-Yehudah
    • 1
    • 3
    Email author
  • Sara Guediche
    • 2
    • 3
  • Julie A. Fiez
    • 1
    • 2
    • 3
  1. 1.Department of PsychologyUniversity of PittsburghUSA
  2. 2.Center for NeuroscienceUniversity of PittsburghUSA
  3. 3.Center for the Neural Basis of CognitionPittsburghUSA

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