Skip to main content
SpringerLink
Log in

Effects of Cerebellar Stimulation on Processing Semantic Associations

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

Current research in cerebellar cognitive and linguistic functions makes plausible the idea that the cerebellum is involved in processing temporally contiguous linguistic input. In order to assess this hypothesis, a lexical decision task was constructed to study the effects of cerebellar transcranial magnetic stimulation on semantic noun-to-verb priming based on association (e.g. ‘soap–cleaning’) or similarity (e.g. ‘robbery–stealing’). The results demonstrated a selective increase in associative priming size after stimulation of a lateral cerebellar site. The findings are discussed in the contexts of a cerebellar role in linguistic expectancy generation and the corticocerebellar ‘prefrontal’ reciprocal loop.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Notes

  1. A simple node-counting scheme (path). The relatedness score is inversely proportional to the number of nodes along the shortest path between the synsets. The shortest possible path occurs when the two synsets are the same, in which case the length is 1. Thus, the maximum relatedness value is 1.

  2. As the software cannot assess the semantic relatedness of words of different grammatical categories (here, nouns and verbs), it was ensured that, in each pair, the noun was homonymous with a verb of the same basic semantic properties, e.g. ‘release’, ‘fear’.

  3. Of course, semantic associative relatedness implies that the forms may co-occur, be it in a non-immediate fashion. However, such loose co-occurrences could easily be found in the categorically related pairs as well. For example, in (1) below, the semantic associatively related pair ‘stripper-entertaining’ (a) can loosely co-occur in speech, like the semantic categorically related one ‘murder-killing’ (b).

    (a)‘[…] being a male stripper isn’t just about taking clothes off, it’s about entertaining people […]’

    (b)‘It would seem that one is guilty of murder through killing someone by chance […]’ (Google search)

  4. Indeed, the priming sizes of the three participants that had participated in earlier versions of this task were significantly larger overall than those of the rest of the no TMS subjects (Relatedness × Experience with task: F (1, 43) = 5.09, MSe = 342.85, p < 0.03; a large priming effect for the Experienced group: Relatedness: F (1, 1) = 19,063.58, MSe = 0.20, p < 0.005).

  5. Distribution of subjects across lists: list A: n = 12; list B: n = 13; list C: n = 11; list D: n = 10; lateral group: A 3; B 3; C 3; D 3; medial group: A 3; B 4; C 2; D 2; no TMS group 1: A 3; B 3; C 3; D 3; no TMS group 2: A 3; B 3; C 3; D 2.

Abbreviations

ANOVA:

Analysis of variance

cm:

Centimetre

mm:

Millimetre

ms:

Millisecond(s)

(r)TMS:

(Repetitive) transcranial magnetic stimulation

SD:

Standard deviation

SEM:

Standard error of the mean

BNC:

British National Corpus

References

  1. Argyropoulos GP. Neocerebellar emulation in language processing. In: Alter K, Horne M, Lindgren M, Roll M, von Koss Torkildsen J, editors. Brain talk: discourse with and in the brain. Papers from the first Birgit Rausing language program conference in linguistics. Lund: Lund University, Media Tryck; 2009. p. 193–206.

    Google Scholar 

  2. Argyropoulos GP. Cerebellar theta-burst stimulation selectively enhances lexical associative priming. Cerebellum. 2011;10(3):540–50.

    Article  PubMed  Google Scholar 

  3. Argyropoulos GP. Cortico-cortical and cortico-cerebellar computations in language change. In: Scott-Phillips TC, Tamariz M, Cartmill EA, Hurford JR, editors. The evolution of language: proceedings of the 7th international conference on the evolution of language. Singapore: World Scientific; 2012. p. 11–8.

    Google Scholar 

  4. Argyropoulos GP, Kimiskidis V, Papagiannopoulos S. Theta-burst stimulation of the right neocerebellar vermis selectively disrupts the practice-induced acceleration of lexical decisions. Behav Neurosci. 2011;125(5):724–34.

    Article  PubMed  Google Scholar 

  5. Bellebaum C, Daum I. Mechanisms of cerebellar involvement in associative learning. Cortex. 2011;47:128–36.

    Article  PubMed  Google Scholar 

  6. Canavan AG, Sprengelmeyer R, Diener HC, Hömberg V. Conditional associative learning is impaired in cerebellar disease in humans. Behav Neurosci. 1994;108:475–85.

    Article  PubMed  CAS  Google Scholar 

  7. Christian KM, Thompson RF. Long-term storage of an associative memory trace in the cerebellum. Behav Neurosci. 2005;119:526–37.

    Article  PubMed  Google Scholar 

  8. Courchesne E, Allen G. Prediction and preparation, fundamental functions of the cerebellum. Learn Mem. 1997;4:1–35.

    Article  PubMed  CAS  Google Scholar 

  9. Daum I, Ackermann H, Schugens MM, Reimold C, Dichgans J, Birbaumer N. The cerebellum and cognitive functions in humans. Behav Neurosci. 1993;107:411–9.

    Article  PubMed  CAS  Google Scholar 

  10. Del Olmo MF, Cheeran B, Koch G, Rothwell JC. Role of the cerebellum in externally paced rhythmic finger movements. J Neurophysiol. 2007;98:145–52.

    Article  PubMed  Google Scholar 

  11. Demirtas-Tatlidede A, Freitas C, Cromer JR, Safar L, Ongur D, Stone WS, Seidman LJ, Schmahmann JD, Pascual-Leone A. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res. 2010;124:91–100.

    Article  PubMed  Google Scholar 

  12. Devlin JT, Watkins KE. Stimulating language: insights from TMS. Brain. 2007;130:610–22.

    Article  PubMed  Google Scholar 

  13. Drepper J, Timmann D, Kolb FP, Diener HC. Non- motor associative learning in patients with isolated degenerative cerebellar disease. Brain. 1999;122:87–97.

    Article  PubMed  Google Scholar 

  14. Fellbaum C (ed) (1998) WordNet: an electronic lexical database. Cambridge: MIT. http://wordnet.princeton.edu/

  15. Ferretti TR, McRae K, Hatherell A. Integrating verbs, situation schemas, and thematic role concepts. J Mem Lang. 2001;44:516–47.

    Article  Google Scholar 

  16. Ferretti TR, Gagné C, McRae K. Thematic role focusing by participle inflections: evidence from conceptual combination. J Exp Psychol Learn Mem Cogn. 2003;29(1):118–27.

    Article  PubMed  Google Scholar 

  17. Ferretti TR, Kutas M, McRae K. Verb aspect and the activation of event knowledge. J Exp Psychol Learn Mem Cogn. 2007;33(1):182–96.

    Article  PubMed  Google Scholar 

  18. Ferrucci R, Marceglia S, Vergari M, Cogiamanian F, Mrakic-Sposta S, Mameli F, Zago S, Barbieri S, Priori A. Cerebellar transcranial direct current stimulation impairs the practice-dependent proficiency increase in working memory. J Cogn Neurosci. 2008;20:1687–97.

    Article  PubMed  CAS  Google Scholar 

  19. Fierro B, Giglia G, Palermo A, Pecoraro C, Scalia S, Brighina F. Modulatory effects of 1 Hz rTMS over the cerebellum on motor cortex excitability. Exp Brain Res. 2007;176:440–7.

    Article  PubMed  Google Scholar 

  20. 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;115:155–78.

    Article  PubMed  Google Scholar 

  21. Fiez JA, Raichle M. Linguistic processing. Int Rev Neurobiol. 1997;41:233–54.

    Article  PubMed  CAS  Google Scholar 

  22. Forster KI, Davis C. The density constraint on form-priming in the naming task: interference from a masked prime. J Mem Lang. 1991;30:1–25.

    Article  Google Scholar 

  23. Frings M, Dimitrova A, Schorn CF, Elles H-G, Hein-Kropp C, Gizewski ER, Diener HC, Timmann D. Cerebellar involvement in verb generation: an fMRI study. Neurosci Lett. 2006;409:19–23.

    Article  PubMed  CAS  Google Scholar 

  24. Gebhart AL, Petersen SE, Thach WT. Role of the posterolateral cerebellum in language. Ann NY Acad Sci. 2002;978:318–33.

    Article  PubMed  Google Scholar 

  25. Hagoort P. Semantic priming in Broca’s aphasics at a short SOA: no support for an automatic access deficit. Brain Lang. 1997;56:287–300.

    Article  PubMed  CAS  Google Scholar 

  26. Hashimoto M, Ohtsuka K. Transcranial magnetic stimulation over the posterior cerebellum during visual saccades in man. Brain. 1995;118:1185–93.

    Article  PubMed  Google Scholar 

  27. Huang Y, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron. 2005;45:201–6.

    Article  PubMed  CAS  Google Scholar 

  28. Jarvis BG. DirectRT (Version 2008.1.0.11) [Computer software]. New York: Empirisoft Corporation; 2008.

    Google Scholar 

  29. Kalla R, Muggleton NG, Cowey A, Walsh V. Human dorsolateral prefrontal cortex is involved in visual search for conjunctions but not features: a theta TMS study. Cortex. 2009;45:1085–109.

    Article  PubMed  Google Scholar 

  30. Kelly RM, Strick PL. Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primate. J Neurosci. 2003;23:8432–44.

    PubMed  CAS  Google Scholar 

  31. Koch G, Mori F, Marconi B, Codecà C, Pecchioli C, Salerno, Torriero S, Lo Gerfo E, Mir P, Oliveri M, Caltagirone C. Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clin Neurophysiol. 2008;119:2559–69.

    Article  PubMed  Google Scholar 

  32. Koch G, Brusa L, Carrillo F, Lo Gerfo E, Torriero S, Oliveri M, Mir P, Caltagirone C, Stanzione P. Cerebellar magnetic stimulation decreases levodopa-induced dyskinesias in Parkinson disease. Neurology. 2009;73:113–9.

    Article  PubMed  CAS  Google Scholar 

  33. Larsell O, Jansen J. The comparative anatomy and histology of the cerebellum, Vol 3 III: the human cerebellum, cerebellar connections, and cerebellar cortex. Minneapolis: University of Minnesota Press; 1972.

    Google Scholar 

  34. Leech G. 100 million words of English: the British National Corpus. Lang Res. 1992;28(1):1–13.

    Google Scholar 

  35. Leggio MG, Silveri MC, Petrosini L, Molinari M. Phonological grouping is specifically affected in cerebellar patients: a verbal fluency study. J Neurol Neurosurg Psychiatry. 2000;69:102–6.

    Article  PubMed  CAS  Google Scholar 

  36. Liu CL, Tseng P, Chiau HY, Liang WK, Hung DL, Tzeng OJ, Muggleton NG, Juan CH. The location probability effects of saccade reaction times are modulated in the frontal eye fields but not in the supplementary eye field. Cereb Cortex. 2010;21(6):1416–25.

    Article  PubMed  Google Scholar 

  37. McCormick DA, Thompson RF. Cerebellum: essential involvement in the classically conditioned eyelid response. Science. 1984;223:296–9.

    Article  PubMed  CAS  Google Scholar 

  38. McRae K, Hare M, Elman JL, Ferretti T. A basis for generating expectancies for verbs from nouns. Mem Cognit. 2005;33:1174–84.

    Article  PubMed  Google Scholar 

  39. Miall RC, King D. State estimation in the cerebellum. Cerebellum. 2008;7:572–6.

    Article  PubMed  Google Scholar 

  40. Middleton FA, Strick PL. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci. 2001;21:700–12.

    PubMed  CAS  Google Scholar 

  41. Moss HE, Ostrin RK, Tyler LK, Marslen-Wilson WD. Accessing different types of lexical semantic information: evidence from priming. J Exp Psychol Learn Mem Cogn. 1995;21(4):863–83.

    Article  Google Scholar 

  42. Ober B. RT and non-RT methodology for semantic priming research with Alzheimer’s disease patients: a critical review. J Clin Exp Neuropsychol. 2002;24:883–911.

    Article  PubMed  Google Scholar 

  43. Ohtsuka K, Enoki T. Transcranial magnetic stimulation over the posterior cerebellum during smooth pursuit eye movements in man. Brain. 1998;121:429–35.

    Article  PubMed  Google Scholar 

  44. Oliveri M, Koch G, Torriero S, Caltagirone C. Increased facilitation of the primary motor cortex following 1 Hz repetitive transcranial magnetic stimulation of the contralateral cerebellum in normal humans. Neurosci Lett. 2005;376:188–93.

    Article  PubMed  CAS  Google Scholar 

  45. Oliveri M, Torriero S, Koch G, Salerno S, Petrosini L, Caltagirone C. The role of transcranial magnetic stimulation in the study of cerebellar cognitive function. Cerebellum. 2007;6:95–101.

    Article  PubMed  Google Scholar 

  46. Oliveri M, Bonni S, Turriziani P, Koch G, Lo Gerfo E, Torriero S, Vicario CM, Petrosini L, Caltagirone C. Motor and linguistic linking of space and time in the cerebellum. PLoS One. 2009;4(11):e7933.

    Article  PubMed  Google Scholar 

  47. Palmer ED, Rosen HJ, Ojemann JG, Buckner RL, Kelley WM, Petersen SE. An event-related fMRI study of overt and covert word stem completion. NeuroImage. 2001;14:182–93.

    Article  PubMed  CAS  Google Scholar 

  48. Paulin M. Neural representations of moving systems. In: Schmahmann JD, editor. The cerebellum and cognition, international review of neurobiology, vol. 41. San Diego: Academic; 1997. p. 515–33.

    Google Scholar 

  49. Pedersen T, Patwardhan S, Michelizzi J. WordNet::similarity—measuring the relatedness of concepts. AAAI. 2004;04:1024–5.

    Google Scholar 

  50. Perea M, Gotor A. Associative and semantic priming effects occur at very short stimulus-onset asynchronies in lexical decision and naming. Cognition. 1997;62:223–40.

    Article  PubMed  CAS  Google Scholar 

  51. Perea M, Rosa E. The effects of associative and semantic priming in the lexical decision task. Psychol Res. 2002;66:180–94.

    Article  PubMed  Google Scholar 

  52. Petersen SE, Fox PT, Posner ML, Mintun M, Raichle ME. Positron emission tomographic studies of the processing of single words. J Cogn Neurosci. 1989;1:153–70.

    Article  Google Scholar 

  53. Pollatsek A, Well AD. On the use of counterbalanced designs in cognitive research: a suggestion for a better and more powerful analysis. J Exp Psychol Learn Mem Cogn. 1995;21:785–94.

    Article  PubMed  CAS  Google Scholar 

  54. Ramnani N. The primate cortico-cerebellar system: anatomy and function. Nat Rev Neurosci. 2006;7:511–22.

    Article  PubMed  CAS  Google Scholar 

  55. Rogers SL, Friedman RB. The underlying mechanisms of semantic memory in Alzheimer’s disease and semantic dementia. Neuropsychologia. 2008;46:12–21.

    Article  PubMed  Google Scholar 

  56. Sack AT. Transcranial magnetic stimulation, causal structure–function mapping and networks of functional relevance. Curr Opin Neurobiol. 2006;16:593–9.

    Article  PubMed  CAS  Google Scholar 

  57. Sack AT, Kadosh RC, Schuhmann T, Moerel M, Walsh V, Goebel R. Optimizing functional accuracy of TMS in cognitive studies: a comparison of methods. J Cogn Neurosci. 2008;21(2):207–21.

    Article  Google Scholar 

  58. Schmahmann JD. The role of the cerebellum in affect and psychosis. J Neurolinguistics. 2000;13:189–214.

    Article  Google Scholar 

  59. Stewart LM, Walsh V, Rothwell JC. Motor and phosphine thresholds: a transcranial magnetic stimulation correlation study. Neuropsychologia. 2001;39:415–9.

    Article  PubMed  CAS  Google Scholar 

  60. Théoret H, Haque J, Pascual-Leone A. Increased variability of paced finger tapping accuracy following repetitive magnetic stimulation of the cerebellum in humans. Neurosci Lett. 2001;306:29–32.

    Article  PubMed  Google Scholar 

  61. Thompson-Schill SL, Kurtz KJ, Gabrieli JDE. Effects of semantic and associative relatedness on automatic priming. J Mem Lang. 1998;38:440–58.

    Article  Google Scholar 

  62. Timmann D, Drepper J, Calabrese S, Bürgerhoff K, Maschke M, Kolb FP, Daum I, Diener HC. Use of sequence information in associative learning in control subjects and cerebellar patients. Cerebellum. 2004;3:75–82.

    Article  PubMed  CAS  Google Scholar 

  63. Timmann D, Drepper J, Frings M, Maschke M, Richter S, Gerwig M, Kolb FP. The human cerebellum contributes to motor, emotional and cognitive associative learning. A review. Cortex. 2010;46:845–57.

    Article  PubMed  CAS  Google Scholar 

  64. Timmann D, Drepper J, Maschke M, Kolb FP, Böring D, Thilmann AF, Diener HC. Motor deficits cannot explain impaired cognitive associative learning in cerebellar patients. Neuropsychologia. 2002;40:788–800.

    Article  PubMed  Google Scholar 

  65. Torriero S, Oliveri M, Koch G, Caltagirone C, Petrosini L. Interference of left and right cerebellar rTMS with procedural learning. J Cogn Neurosci. 2004;16:1605–11.

    Article  PubMed  Google Scholar 

  66. Torriero S, Oliveri M, Koch G, Lo Gerfo E, Salerno S, Petrosini L, Caltagirone C. Cortical networks of procedural learning: evidence from cerebellar damage. Neuropsychologia. 2007;45:1208–14.

    Article  PubMed  Google Scholar 

  67. Torriero S, Oliveri M, Koch G, Lo Gerfo E, Salerno S, Ferlazzo F, Caltagirone C, Petrosini L. Changes in cerebello-motor connectivity during procedural learning by actual execution and observation. J Cogn Neurosci. 2010;23(2):338–48.

    Article  PubMed  Google Scholar 

  68. Tucker J, Harding AE, Jahanshahi M, Nixon PD, Rushworth M, Quinn NP, Thompson PD, Passingham RE. Associative learning in patients with cerebellar ataxia. Behav Neurosci. 1996;110:1229–34.

    Article  PubMed  CAS  Google Scholar 

  69. Ugawa Y, Uesaka Y, Terao Y, Hanajima R, Kanazawa I. Magnetic stimulation over the cerebellum in humans. Ann Neurol. 1995;37:703–13.

    Article  PubMed  CAS  Google Scholar 

  70. Vallesi A, Shallice T, Walsh V. Role of the prefrontal cortex in the foreperiod effect: TMS evidence for dual mechanisms in temporal preparation. Cereb Cortex. 2007;17:466–74.

    Article  PubMed  Google Scholar 

  71. Wolpert DM, Miall RC, Kawato M. Internal models in the cerebellum. Trends Cogn Sci. 1998;2:338–47.

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Dr. Thomas Bak, Prof. Simon Garrod, Prof. Jim Hurford, Prof. Vassilios Kimiskidis, Prof. Maria Leggio, Prof. Ken McRae, Prof. Massimo Oliveri, Prof. Martin Pickering, Prof. Richard Shillcock, Prof. Steve Small, Prof Ana Solodkin, Dr. Patrick Sturt, as well as the reviewers of the journal for their precious support and encouragement. NGM was supported by the UK Medical Research Council and by the National Science Council, Taiwan (100-2410-H-008-074-MY3).

Conflict of Interest

There were no conflicts of interest.

Author information

Authors and Affiliations

  1. Language Evolution and Computation Research Unit, Linguistics and English Language, School of Philosophy, Psychology and Language Sciences, University of Edinburgh, 3 Charles Street, Edinburgh, EH8 9AD, UK

    Giorgos P. Argyropoulos

  2. Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London, WC1N 3AR, UK

    Neil G. Muggleton

  3. Institute of Cognitive Neuroscience, National Central University, Jhongli, 320, Taiwan

    Neil G. Muggleton

  4. Laboratories for Cognitive Neuroscience, National Yang-Ming University, Taipei, 112, Taiwan

    Neil G. Muggleton

Authors
  1. Giorgos P. Argyropoulos
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Neil G. Muggleton
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giorgos P. Argyropoulos.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Argyropoulos, G.P., Muggleton, N.G. Effects of Cerebellar Stimulation on Processing Semantic Associations. Cerebellum 12, 83–96 (2013). https://doi.org/10.1007/s12311-012-0398-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-012-0398-y

Keywords

Search

Navigation