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. 2002 Sep 22;269(1503):1895–1904. doi: 10.1098/rspb.2002.2103

Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex.

Paul Dean 1, John Porrill 1, James V Stone 1
PMCID: PMC1691115  PMID: 12350251

Abstract

We introduce decorrelation control as a candidate algorithm for the cerebellar microcircuit and demonstrate its utility for oculomotor plant compensation in a linear model of the vestibulo-ocular reflex (VOR). Using an adaptive-filter representation of cerebellar cortex and an anti-Hebbian learning rule, the algorithm learnt to compensate for the oculomotor plant by minimizing correlations between a predictor variable (eye-movement command) and a target variable (retinal slip), without requiring a motor-error signal. Because it also provides an estimate of the unpredicted component of the target variable, decorrelation control can simplify both motor coordination and sensory acquisition. It thus unifies motor and sensory cerebellar functions.

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Selected References

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  1. Barnes G. R., Asselman P. T. The mechanism of prediction in human smooth pursuit eye movements. J Physiol. 1991 Aug;439:439–461. doi: 10.1113/jphysiol.1991.sp018675. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bell C., Bodznick D., Montgomery J., Bastian J. The generation and subtraction of sensory expectations within cerebellum-like structures. Brain Behav Evol. 1997;50 (Suppl 1):17–31. doi: 10.1159/000113352. [DOI] [PubMed] [Google Scholar]
  3. Belton T., McCrea R. A. Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation. J Neurophysiol. 2000 Sep;84(3):1599–1613. doi: 10.1152/jn.2000.84.3.1599. [DOI] [PubMed] [Google Scholar]
  4. Blakemore S. J., Wolpert D., Frith C. Why can't you tickle yourself? Neuroreport. 2000 Aug 3;11(11):R11–R16. doi: 10.1097/00001756-200008030-00002. [DOI] [PubMed] [Google Scholar]
  5. Büttner-Ennever J. A., Horn A. K. Pathways from cell groups of the paramedian tracts to the floccular region. Ann N Y Acad Sci. 1996 Jun 19;781:532–540. doi: 10.1111/j.1749-6632.1996.tb15726.x. [DOI] [PubMed] [Google Scholar]
  6. De Zeeuw C. I., Wylie D. R., Stahl J. S., Simpson J. I. Phase relations of Purkinje cells in the rabbit flocculus during compensatory eye movements. J Neurophysiol. 1995 Nov;74(5):2051–2064. doi: 10.1152/jn.1995.74.5.2051. [DOI] [PubMed] [Google Scholar]
  7. Devor A. Is the cerebellum like cerebellar-like structures? Brain Res Brain Res Rev. 2000 Dec;34(3):149–156. doi: 10.1016/s0165-0173(00)00045-x. [DOI] [PubMed] [Google Scholar]
  8. Fuchs A. F., Scudder C. A., Kaneko C. R. Discharge patterns and recruitment order of identified motoneurons and internuclear neurons in the monkey abducens nucleus. J Neurophysiol. 1988 Dec;60(6):1874–1895. doi: 10.1152/jn.1988.60.6.1874. [DOI] [PubMed] [Google Scholar]
  9. Fujita M. Adaptive filter model of the cerebellum. Biol Cybern. 1982;45(3):195–206. doi: 10.1007/BF00336192. [DOI] [PubMed] [Google Scholar]
  10. Fujita M. Simulation of adaptive modification of the vestibulo-ocular reflex with an adaptive filter model of the cerebellum. Biol Cybern. 1982;45(3):207–214. doi: 10.1007/BF00336193. [DOI] [PubMed] [Google Scholar]
  11. Fukushima K., Kaneko C. R. Vestibular integrators in the oculomotor system. Neurosci Res. 1995 Jun;22(3):249–258. doi: 10.1016/0168-0102(95)00904-8. [DOI] [PubMed] [Google Scholar]
  12. Gilbert P. F. A theory of memory that explains the function and structure of the cerebellum. Brain Res. 1974 Apr 12;70(1):1–18. doi: 10.1016/0006-8993(74)90208-x. [DOI] [PubMed] [Google Scholar]
  13. Gomi H., Kawato M. Adaptive feedback control models of the vestibulocerebellum and spinocerebellum. Biol Cybern. 1992;68(2):105–114. doi: 10.1007/BF00201432. [DOI] [PubMed] [Google Scholar]
  14. Hartmann M. J., Bower J. M. Tactile responses in the granule cell layer of cerebellar folium crus IIa of freely behaving rats. J Neurosci. 2001 May 15;21(10):3549–3563. doi: 10.1523/JNEUROSCI.21-10-03549.2001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ito M. Neurophysiological aspects of the cerebellar motor control system. Int J Neurol. 1970;7(2):162–176. [PubMed] [Google Scholar]
  16. Kettner R. E., Mahamud S., Leung H. C., Sitkoff N., Houk J. C., Peterson B. W., Barto A. G. Prediction of complex two-dimensional trajectories by a cerebellar model of smooth pursuit eye movement. J Neurophysiol. 1997 Apr;77(4):2115–2130. doi: 10.1152/jn.1997.77.4.2115. [DOI] [PubMed] [Google Scholar]
  17. Leung H. C., Suh M., Kettner R. E. Cerebellar flocculus and paraflocculus Purkinje cell activity during circular pursuit in monkey. J Neurophysiol. 2000 Jan;83(1):13–30. doi: 10.1152/jn.2000.83.1.13. [DOI] [PubMed] [Google Scholar]
  18. Lisberger S. G., Fuchs A. F. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. I. Purkinje cell activity during visually guided horizontal smooth-pursuit eye movements and passive head rotation. J Neurophysiol. 1978 May;41(3):733–763. doi: 10.1152/jn.1978.41.3.733. [DOI] [PubMed] [Google Scholar]
  19. Lisberger S. G. Physiologic basis for motor learning in the vestibulo-ocular reflex. Otolaryngol Head Neck Surg. 1998 Jul;119(1):43–48. doi: 10.1016/S0194-5998(98)70172-X. [DOI] [PubMed] [Google Scholar]
  20. Marr D. A theory of cerebellar cortex. J Physiol. 1969 Jun;202(2):437–470. doi: 10.1113/jphysiol.1969.sp008820. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Medina J. F., Mauk M. D. Computer simulation of cerebellar information processing. Nat Neurosci. 2000 Nov;3 (Suppl):1205–1211. doi: 10.1038/81486. [DOI] [PubMed] [Google Scholar]
  22. Middleton F. A., Strick P. L. Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev. 2000 Mar;31(2-3):236–250. doi: 10.1016/s0165-0173(99)00040-5. [DOI] [PubMed] [Google Scholar]
  23. Nakamagoe K., Iwamoto Y., Yoshida K. Evidence for brainstem structures participating in oculomotor integration. Science. 2000 May 5;288(5467):857–859. doi: 10.1126/science.288.5467.857. [DOI] [PubMed] [Google Scholar]
  24. Nelson M. E., Paulin M. G. Neural simulations of adaptive reafference suppression in the elasmobranch electrosensory system. J Comp Physiol A. 1995 Dec;177(6):723–736. doi: 10.1007/BF00187631. [DOI] [PubMed] [Google Scholar]
  25. Nixon P. D., Passingham R. E. Predicting sensory events. The role of the cerebellum in motor learning. Exp Brain Res. 2001 May;138(2):251–257. doi: 10.1007/s002210100702. [DOI] [PubMed] [Google Scholar]
  26. Noda H., Suzuki D. A. The role of the flocculus of the monkey in fixation and smooth pursuit eye movements. J Physiol. 1979 Sep;294:335–348. doi: 10.1113/jphysiol.1979.sp012933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Optican L. M., Miles F. A. Visually induced adaptive changes in primate saccadic oculomotor control signals. J Neurophysiol. 1985 Oct;54(4):940–958. doi: 10.1152/jn.1985.54.4.940. [DOI] [PubMed] [Google Scholar]
  28. Optican L. M., Zee D. S., Miles F. A. Floccular lesions abolish adaptive control of post-saccadic ocular drift in primates. Exp Brain Res. 1986;64(3):596–598. doi: 10.1007/BF00340497. [DOI] [PubMed] [Google Scholar]
  29. Paulin M. G. The role of the cerebellum in motor control and perception. Brain Behav Evol. 1993;41(1):39–50. doi: 10.1159/000113822. [DOI] [PubMed] [Google Scholar]
  30. Raymond J. L., Lisberger S. G. Neural learning rules for the vestibulo-ocular reflex. J Neurosci. 1998 Nov 1;18(21):9112–9129. doi: 10.1523/JNEUROSCI.18-21-09112.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Roberts P. D., Bell C. C. Computational consequences of temporally asymmetric learning rules: II. Sensory image cancellation. J Comput Neurosci. 2000 Jul-Aug;9(1):67–83. doi: 10.1023/a:1008938428112. [DOI] [PubMed] [Google Scholar]
  32. Sejnowski T. J. Storing covariance with nonlinearly interacting neurons. J Math Biol. 1977 Oct 20;4(4):303–321. doi: 10.1007/BF00275079. [DOI] [PubMed] [Google Scholar]
  33. Suh M., Leung H. C., Kettner R. E. Cerebellar flocculus and ventral paraflocculus Purkinje cell activity during predictive and visually driven pursuit in monkey. J Neurophysiol. 2000 Oct;84(4):1835–1850. doi: 10.1152/jn.2000.84.4.1835. [DOI] [PubMed] [Google Scholar]
  34. Wang S. S., Denk W., Häusser M. Coincidence detection in single dendritic spines mediated by calcium release. Nat Neurosci. 2000 Dec;3(12):1266–1273. doi: 10.1038/81792. [DOI] [PubMed] [Google Scholar]
  35. Zee D. S., Yamazaki A., Butler P. H., Gücer G. Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol. 1981 Oct;46(4):878–899. doi: 10.1152/jn.1981.46.4.878. [DOI] [PubMed] [Google Scholar]

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