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The Cerebellum

, Volume 13, Issue 1, pp 46–54 | Cite as

Effects of Attention and Perceptual Uncertainty on Cerebellar Activity During Visual Motion Perception

  • Oliver BaumannEmail author
  • Jason B. Mattingley
Original Paper

Abstract

Recent clinical and neuroimaging studies have revealed that the human cerebellum plays a role in visual motion perception, but the nature of its contribution to this function is not understood. Some reports suggest that the cerebellum might facilitate motion perception by aiding attentive tracking of visual objects. Others have identified a particular role for the cerebellum in discriminating motion signals in perceptually uncertain conditions. Here, we used functional magnetic resonance imaging to determine the degree to which cerebellar involvement in visual motion perception can be explained by a role in sustained attentive tracking of moving stimuli in contrast to a role in visual motion discrimination. While holding the visual displays constant, we manipulated attention by having participants attend covertly to a field of random-dot motion or a colored spot at fixation. Perceptual uncertainty was manipulated by varying the percentage of signal dots contained within the random-dot arrays. We found that attention to motion under high perceptual uncertainty was associated with strong activity in left cerebellar lobules VI and VII. By contrast, attending to motion under low perceptual uncertainty did not cause differential activation in the cerebellum. We found no evidence to support the suggestion that the cerebellum is involved in simple attentive tracking of salient moving objects. Instead, our results indicate that specific subregions of the cerebellum are involved in facilitating the detection and discrimination of task-relevant moving objects under conditions of high perceptual uncertainty. We conclude that the cerebellum aids motion perception under conditions of high perceptual demand.

Keywords

Cerebellum fMRI Perception Attention Motion Uncertainty 

Notes

Acknowledgments

This work was supported by an Australian Research Council Discovery Early Career Researcher Award (DE120100535), a UQ Foundation Research Excellence Award and a UQ Early Career Researcher Grant to OB. JBM was supported by an Australian Research Council Australian Laureate Fellowship (FL110100103).

Conflicts of Interest

The authors declare that no financial or personal competing interests exist.

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References

  1. 1.
    Paulin MG. The role of the cerebellum on motor control and perception. Brain Behav Evol. 1993;41:39–50.PubMedCrossRefGoogle Scholar
  2. 2.
    Schmahmann JD. The cerebrocerebellar system: anatomic substrates of the cerebellar contribution to cognition and emotion. Int Rev Psychiatry. 2001;13:247–60.CrossRefGoogle Scholar
  3. 3.
    Bastian AJ. Moving, sensing and learning with cerebellar damage. Curr Opin Neurobiol. 2011;21:596–601.PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Thier P, Haarmeier T, Treue S, Barash S. Absence of a common functional denominator of visual disturbances in cerebellar disease. Brain. 1999;122:2133–46.PubMedCrossRefGoogle Scholar
  5. 5.
    Jokisch D, Troje NF, Koch B, Schwarz M, Daum I. Differential involvement of the cerebellum in biological and coherent motion perception. Eur J Neurosci. 2005;21:3439–46.PubMedCrossRefGoogle Scholar
  6. 6.
    Bower JM. Control of sensory data acquisition. In: Schmahmann JD, editor. The cerebellum and cognition. San Diego: Academic; 2007. p. 489–513.Google Scholar
  7. 7.
    Bower JM. The organization of cerebellar cortical circuitry revisited: implications for function. Ann N Y Acad Sci. 2002;978:135–55.PubMedCrossRefGoogle Scholar
  8. 8.
    Bower JM. Computational structure of the cerebellar molecular layer. In: Manto M, Gruol D, Schmahmann J, Koibuchi N, Rossi F, editors. Handbook of the cerebellum and cerebellar disorders. New York: Springer; 2013. p. 1359–80.CrossRefGoogle Scholar
  9. 9.
    Baumann O, Mattingley JB. Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci. 2010;30:4489–95.PubMedCrossRefGoogle Scholar
  10. 10.
    Jovicich J, Peters RJ, Koch C, Braun J, Chang L, Ernst T. Brain areas specific for attentional load in a motion-tracking task. J Cogn Neurosci. 2001;13:1048–58.PubMedCrossRefGoogle Scholar
  11. 11.
    Thakral PP, Slotnick SD. The role of parietal cortex during sustained visual spatial attention. Brain Res. 2009;1402:157–66.CrossRefGoogle Scholar
  12. 12.
    Jahn G, Wendt J, Lotze M, Papenmeier F, Huff M. Brain activation during spatial updating and attentive tracking of moving targets. Brain Cogn. 2012;78:105–13.PubMedCrossRefGoogle Scholar
  13. 13.
    Kellermann T, Regenbogen C, De Vos M, Mößnang C, Finkelmeyer A, Habel U. Effective connectivity of the human cerebellum during visual attention. J Neurosci. 2012;32:11453–60.PubMedCrossRefGoogle Scholar
  14. 14.
    Dale AM. Optimal experimental design for event-related fMRI. Hum Brain Mapp. 1999;8:109–14.PubMedCrossRefGoogle Scholar
  15. 15.
    Zeng H, Constable RT. Image distortion correction in EPI: comparison of field mapping with point spread function mapping. Magn Reson Med. 2002;48:137–46.PubMedCrossRefGoogle Scholar
  16. 16.
    Zaitsev M, Steinhoff S, Shah NJ. Error reduction and parameter optimization of the TAPIR method for fast T1 mapping. Magn Reson Med. 2003;49:1121–32.PubMedCrossRefGoogle Scholar
  17. 17.
    Glover GH, Li TQ, Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn Reson Med. 2000;44:162–7.PubMedCrossRefGoogle Scholar
  18. 18.
    Shmueli K, Van Gelderen P, de Zwart JA, Horovitz SG, Fukunaga M, Jansma JM, et al. Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal. Neuroimage. 2007;8:306–20.CrossRefGoogle Scholar
  19. 19.
    Birn RM, Smith MA, Jones TB, Bandettini PA. The respiration response function: the temporal dynamics of fMRI signal fluctuations related to changes in respiration. Neuroimage. 2008;40:644–54.PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    Chang C, Cunningham JP, Glover GH. Influence of heart rate on the BOLD signal: the cardiac response function. Neuroimage. 2009;44:857–69.PubMedCentralPubMedCrossRefGoogle Scholar
  21. 21.
    Verstynen TD, Deshpande V. Using pulse oximetry to account for high and low frequency physiological artifacts in the BOLD signal. Neuroimage. 2011;55:1633–44.PubMedCrossRefGoogle Scholar
  22. 22.
    Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. Neuroimage. 2006;33:127–38.PubMedCrossRefGoogle Scholar
  23. 23.
    Diedrichsen J, Maderwald S, Küper M, Thürling M, Rabe K, Gizewski ER, et al. Imaging the deep cerebellar nuclei: a probabilistic atlas and normalization procedure. Neuroimage. 2011;54:1786–94.PubMedCrossRefGoogle Scholar
  24. 24.
    Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1995;2:189–210.CrossRefGoogle Scholar
  25. 25.
    Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic atlas of the human cerebellum. Neuroimage. 2009;46:39–46.PubMedCrossRefGoogle Scholar
  26. 26.
    Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single subject brain. Neuroimage. 2002;15:273–89.PubMedCrossRefGoogle Scholar
  27. 27.
    Stoodley CJ, Valera EM, Schmahmann JD. Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study. Neuroimage. 2012;59:1560–70.PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    O’Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2010;20:953–65.PubMedCrossRefGoogle Scholar
  29. 29.
    Büchel C, Josephs O, Rees G, Turner R, Frith CD, Friston KJ. The functional anatomy of attention to visual motion. A functional MRI study. Brain. 1998;121:1281–94.PubMedCrossRefGoogle Scholar
  30. 30.
    Culham JC, Brandt SA, Cavanagh P, Kanwisher NG, Dale AM, Tootell RB. Cortical fMRI activation produced by attentive tracking of moving targets. J Neurophysiol. 1998;80:2657–70.PubMedGoogle Scholar
  31. 31.
    Parsons LM, Petacchi A, Schmahmann JD, Bower JM. Pitch discrimination in cerebellar patients: evidence for a sensory deficit. Brain Res. 2009;15:84–96.CrossRefGoogle Scholar
  32. 32.
    Petacchi A, Kaernbach C, Ratnam R, Bower JM. Increased activation of the human cerebellum during pitch discrimination: a positron emission tomography (PET) study. Hear Res. 2011;282:35–48.PubMedCrossRefGoogle Scholar
  33. 33.
    Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci. 2009;29:8586–94.PubMedCentralPubMedCrossRefGoogle Scholar
  34. 34.
    Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:2322–45.PubMedCrossRefGoogle Scholar
  35. 35.
    Shulman GL, McAvoy MP, Cowan MC, Astafiev SV, Tansy AP, d’Avossa G, et al. Quantitative analysis of attention and detection signals during visual search. J Neurophysiol. 2003;90:3384–97.PubMedCrossRefGoogle Scholar
  36. 36.
    Shulman GL, Ollinger JM, Linenweber M, Petersen SE, Corbetta M. Multiple neural correlates of detection in the human brain. Proc Natl Acad Sci U S A. 2001;98:313–8.PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Petacchi A, Laird AR, Fox PT, Bower JM. Cerebellum and auditory function: an ALE meta-analysis of functional neuroimaging studies. Hum Brain Mapp. 2005;25:118–228.PubMedCrossRefGoogle Scholar
  38. 38.
    Lewis JW. Audio-visual perception of everyday natural objects—hemodynamic studies in humans. In: Naumer J, Kaiser J, editors. Multisensory object perception in the primate brain. New York: Springer; 2010.Google Scholar
  39. 39.
    Schmahmann JD. From movement to thought: anatomic substrates of the cerebellar contribution to cognitive processing. Hum Brain Mapp. 1996;4:174–98.PubMedCrossRefGoogle Scholar
  40. 40.
    Baumann O, Ziemus B, Luerding R, Schuierer G, Bogdahn U, Greenlee MW. Differences in cortical activation during smooth pursuit and saccadic eye movements following cerebellar lesions. Exp Brain Res. 2007;181:237–47.PubMedCrossRefGoogle Scholar
  41. 41.
    Leigh JR, Zee DS. The neurology of eye movements. New York: Oxford University Press; 2006.Google Scholar
  42. 42.
    Lynch JC, Tian JR. Cortico-cortical networks and cortico-subcortical loops for the higher control of eye movements. Prog Brain Res. 2006;151:461–501.PubMedCrossRefGoogle Scholar
  43. 43.
    Tanabe J, Tregellas J, Miller D, Ross RG, Freedman R. Brain activation during smooth-pursuit eye movements. Neuroimage. 2002;17:1315–24.PubMedCrossRefGoogle Scholar
  44. 44.
    Dieterich M, Bucher SF, Seelos KC, Brandt T. Cerebellar activation during optokinetic stimulation and saccades. Neurology. 2000;54:148–55.PubMedCrossRefGoogle Scholar
  45. 45.
    Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp. 2001;13:55–73.PubMedCrossRefGoogle Scholar
  46. 46.
    Schlerf J, Ivry RB, Diedrichsen J. Encoding of sensory prediction errors in the human cerebellum. J Neurosci. 2012;32:4504–11.Google Scholar
  47. 47.
    Luft AR, Skalej M, Welte D, Kolb R, Burk K, Schulz JB, et al. A new semiautomated, three-dimensional technique allowing precise quantification of total and regional cerebellar volume using MRI. Magn Reson Med. 1998;40:143–51.PubMedCrossRefGoogle Scholar
  48. 48.
    Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC. MRI atlas of the human cerebellum. San Diego: Academic; 2000.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Queensland Brain InstituteThe University of QueenslandSt LuciaAustralia

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