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Inferior Olive Response to Passive Tactile and Visual Stimulation with Variable Interstimulus Intervals

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Abstract

The unique anatomical and electrophysiological features of the inferior olive and its importance to cerebellar function have been recognized for decades. However, understanding the exact function of the inferior olive has been limited by the general lack of correlation between its neural activity and specific behavioral states. Electrophysiological studies in animals showed that the inferior olive response to sensory stimuli is generally invariant to stimulus properties but is enhanced by unexpected stimuli. Using functional magnetic resonance imaging in humans, we have shown that the inferior olive is activated when subjects performed a task requiring perception of visual stimuli with unpredictable timing (Xu et al. J Neurosci 26(22):5990–5995, 2006, Liu et al. J Neurophysiol 100(3):1557–1561, 2008). In the current study, subjects were scanned while passively perceiving visual and tactile stimuli that were rendered unpredictable by continuously varying interstimulus intervals (ISIs). Sequences of visual stimuli and tactile stimuli to the right hand were presented separately within the same scanning session. In addition to the activation of multiple areas in the cerebellar cortex consistent with previous imaging studies, the results show that both tactile and visual stimulation with variable ISIs were effective in activating the inferior olive. Together with our previous findings, the current results are consistent with the electrophysiological studies in animals and further support the view that the inferior olive and the climbing fiber system primarily convey the temporal information of sensory input regardless of the modality.

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References

  1. Xu D, Liu T, Ashe J, Bushara KO. Role of the olivo-cerebellar system in timing. J Neurosci. 2006;26(22):5990–5.

    Article  CAS  PubMed  Google Scholar 

  2. Liu T, Xu D, Ashe J, Bushara K. Specificity of inferior olive response to stimulus timing. J Neurophysiol. 2008;100(3):1557–61.

    Article  CAS  PubMed  Google Scholar 

  3. Bell CC, Grimm RJ. Discharge properties of Purkinje cells recorded on single and double microelectrodes. J Neurophysiol. 1969;32(6):1044–55.

    CAS  PubMed  Google Scholar 

  4. Llinas R. Motor control: report of the Dahlem workshop on motor control: concepts and issues, Berlin, 1989, December 3–8. In: Humphrey DR, Freund HJ, Freie Universitèat Berlin., Berlin (Germany: West). Senat. & Stifterverband fèur die Deutsche Wissenschaft, editors. Dahlem workshop reports. New York: Wiley, Chichester; 1991. p. 223–242.

    Google Scholar 

  5. Armstrong DM. Functional significance of connections of the inferior olive. Physiol Rev. 1974;54(2):358–417.

    CAS  PubMed  Google Scholar 

  6. Rushmer DS, Roberts WJ, Augter GK. Climbing fiber responses of cerebellar Purkinje cells to passive movement of the cat forepaw. Brain Res. 1976;106(1):1–20.

    Article  CAS  PubMed  Google Scholar 

  7. Ishikawa K, Kawaguchi S, Rowe MJ. Actions of afferent impulses from muscle receptors on cerebellar Purkinje cells: I. Responses to muscle vibration. Exp Brain Res. 1972;15(2):177–93.

    Article  CAS  PubMed  Google Scholar 

  8. Llinas R, Baker R, Sotelo C. Electrotonic coupling between neurons in cat inferior olive. J Neurophysiol. 1974;37(3):560–71.

    CAS  PubMed  Google Scholar 

  9. Llinas R, Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol. 1981;315:549–67.

    CAS  PubMed  Google Scholar 

  10. Bloedel JR, Ebner TJ. Rhythmic discharge of climbing fibre afferents in response to natural peripheral stimuli in the cat. J Physiol. 1984;352:129–46.

    CAS  PubMed  Google Scholar 

  11. Eccles JC, Sabah NH, Schmidt RF, Taborikova H. Cutaneous mechanoreceptors influencing impulse discharges in cerebellar cortex: 3. In Purkinje cells by climbing fiber input. Exp Brain Res. 1972;15(5):484–97.

    Article  CAS  PubMed  Google Scholar 

  12. Gellman R, Gibson AR, Houk JC. Inferior olivary neurons in the awake cat: detection of contact and passive body displacement. J Neurophysiol. 1985;54(1):40–60.

    CAS  PubMed  Google Scholar 

  13. Barmack NH, Simpson JI. Effects of microlesions of dorsal cap of inferior olive of rabbits on optokinetic and vestibuloocular reflexes. J Neurophysiol. 1980;43(1):182–206.

    CAS  PubMed  Google Scholar 

  14. Winkelman B, Frens M. Motor coding in floccular climbing fibers. J Neurophysiol. 2006;95(4):2342–51.

    Article  PubMed  Google Scholar 

  15. Bloedel JR, Bracha V. Current concepts of climbing fiber function. Anat Rec. 1998;253(4):118–26.

    Article  CAS  PubMed  Google Scholar 

  16. Yarom Y, Cohen D. The olivocerebellar system as a generator of temporal patterns. Ann N Y Acad Sci. 2002;978:122–34.

    Article  CAS  PubMed  Google Scholar 

  17. Jacobson GA, Rokni D, Yarom Y. A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci. 2008;31(12):617–25.

    Article  CAS  PubMed  Google Scholar 

  18. Llinas RR. Inferior olive oscillation as the temporal basis for motricity and oscillatory reset as the basis for motor error correction. Neuroscience. 2009;162(3):797–804.

    Article  CAS  PubMed  Google Scholar 

  19. Lidierth M, Apps R. Gating in the spino-olivocerebellar pathways to the c1 zone of the cerebellar cortex during locomotion in the cat. J Physiol. 1990;430:453–69.

    CAS  PubMed  Google Scholar 

  20. Horn KM, Van Kan PL, Gibson AR. Reduction of rostral dorsal accessory olive responses during reaching. J Neurophysiol. 1996;76(6):4140–51.

    CAS  PubMed  Google Scholar 

  21. Gibson AR, Horn KM, Pong M. Inhibitory control of olivary discharge. Ann N Y Acad Sci. 2002;978:219–31.

    Article  PubMed  Google Scholar 

  22. Gellman R, Houk JC, Gibson AR. Somatosensory properties of the inferior olive of the cat. J Comp Neurol. 1983;215(2):228–43.

    Article  CAS  PubMed  Google Scholar 

  23. Gibson AR, Horn KM, Pong M. Activation of climbing fibers. Cerebellum. 2004;3(4):212–21.

    Article  PubMed  Google Scholar 

  24. Diedrichsen J. A spatially unbiased atlas template of the human cerebellum. NeuroImage. 2006;33(1):127–38.

    Article  PubMed  Google Scholar 

  25. Penny W, Holmes A. Random effect analysis. In: FK FRSJ, Frith CD, Dolan R, Price CJ, Zeki S, Ashburner J, Penny WD, editors. Human brain function. New York: Academic; 2003. p. 843–50.

    Google Scholar 

  26. Grodd W, Hulsmann E, Lotze M, Wildgruber D, Erb M. Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotropic organization. Hum Brain Mapp. 2001;13(2):55–73.

    Article  CAS  PubMed  Google Scholar 

  27. Bushara KO, Wheat JM, Khan A, Mock BJ, Turski PA, Sorenson J, et al. Multiple tactile maps in the human cerebellum. NeuroReport. 2001;12(11):2483–6.

    Article  CAS  PubMed  Google Scholar 

  28. Baumann O, Mattingley JB. Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci. 2010;30(12):4489–95.

    Article  CAS  PubMed  Google Scholar 

  29. Price CJ, Friston KJ. Cognitive conjunction: a new approach to brain activation experiments. NeuroImage. 1997;5:261–70.

    Article  CAS  PubMed  Google Scholar 

  30. Marsden CD, Rowland R. The mammalian pons, olive and pyramid. J Comp Neurol. 1965;124:175–87.

    Article  CAS  PubMed  Google Scholar 

  31. Kalil K. Projections of the cerebellar and dorsal column nuclei upon the inferior olive in the rhesus monkey: an autoradiographic study. J Comp Neurol. 1979;188(1):43–62.

    Article  CAS  PubMed  Google Scholar 

  32. Welsh JP, Ahn ES, Placantonakis DG. Is autism due to brain desynchronization? Int J Dev Neurosci. 2005;23(2–3):253–63.

    Article  PubMed  Google Scholar 

  33. Lamarre Y. Tremorgenic mechanisms in primates. Adv Neurol. 1975;10:23–34.

    CAS  PubMed  Google Scholar 

  34. Llinas R, Pare D. Role of intrinsic neuronal oscillations and network ensembles in the genesis of normal and pathological tremors. In: Findley LJ, Koller WC, editors. Handbook of tremor disorders. New York: Marcel Dekker; 1995. p. 7–36.

    Google Scholar 

  35. Schmahmann JD, Doyon J, McDonald D, Holmes C, Lavoie K, Hurwitz AS, et al. Three-dimensional MRI atlas of the human cerebellum in proportional stereotaxic space. NeuroImage. 1999;10:233–60.

    Article  CAS  PubMed  Google Scholar 

  36. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage. 2009;46(1):39–46.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work is supported by the Department Of Veterans Affairs and the International Essential Tremor Foundation.

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For all authors, potential conflicts do not exist.

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Correspondence to K. Bushara.

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Supplementary Table 1

Cortical and subcortical areas activated during tactile and visual stimulation with variable inter-stimulus intervals. R: right, L: left. Cerebellar and brain-stem activations are shown in Table 1. (DOC 60 kb)

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Wu, X., Nestrasil, I., Ashe, J. et al. Inferior Olive Response to Passive Tactile and Visual Stimulation with Variable Interstimulus Intervals. Cerebellum 9, 598–602 (2010). https://doi.org/10.1007/s12311-010-0203-8

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