Abstract
Current views of cerebellar function have been heavily influenced by the models of Marr and Albus, who suggested that the climbing fibre input to the cerebellum acts as a teaching signal for motor learning. It is commonly assumed that this teaching signal must be motor error (the difference between actual and correct motor command), but this approach requires complex neural structures to estimate unobservable motor error from its observed sensory consequences. We have proposed elsewhere a recurrent decorrelation control architecture in which Marr-Albus models learn without requiring motor error. Here, we prove convergence for this architecture and demonstrate important advantages for the modular control of systems with multiple degrees of freedom. These results are illustrated by modelling adaptive plant compensation for the three-dimensional vestibular ocular reflex. This provides a functional role for recurrent cerebellar connectivity, which may be a generic anatomical feature of projections between regions of cerebral and cerebellar cortex.
Full Text
The Full Text of this article is available as a PDF (166.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Andersson G., Garwicz M., Hesslow G. Evidence for a GABA-mediated cerebellar inhibition of the inferior olive in the cat. Exp Brain Res. 1988;72(3):450–456. doi: 10.1007/BF00250590. [DOI] [PubMed] [Google Scholar]
- Barto A. G., Fagg A. H., Sitkoff N., Houk J. C. A cerebellar model of timing and prediction in the control of reaching. Neural Comput. 1999 Apr 1;11(3):565–594. doi: 10.1162/089976699300016575. [DOI] [PubMed] [Google Scholar]
- 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]
- Büttner-Ennever J. A., Cohen B., Horn A. K., Reisine H. Pretectal projections to the oculomotor complex of the monkey and their role in eye movements. J Comp Neurol. 1996 Mar 4;366(2):348–359. doi: 10.1002/(SICI)1096-9861(19960304)366:2<348::AID-CNE12>3.0.CO;2-L. [DOI] [PubMed] [Google Scholar]
- Cheron G., Escudero M., Godaux E. Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. I. Medical vestibular nucleus. J Neurophysiol. 1996 Sep;76(3):1759–1774. doi: 10.1152/jn.1996.76.3.1759. [DOI] [PubMed] [Google Scholar]
- De Zeeuw C. I., Simpson J. I., Hoogenraad C. C., Galjart N., Koekkoek S. K., Ruigrok T. J. Microcircuitry and function of the inferior olive. Trends Neurosci. 1998 Sep;21(9):391–400. doi: 10.1016/s0166-2236(98)01310-1. [DOI] [PubMed] [Google Scholar]
- Dean Paul, Porrill John, Stone James V. Decorrelation control by the cerebellum achieves oculomotor plant compensation in simulated vestibulo-ocular reflex. Proc Biol Sci. 2002 Sep 22;269(1503):1895–1904. doi: 10.1098/rspb.2002.2103. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dum Richard P., Strick Peter L. An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. J Neurophysiol. 2003 Jan;89(1):634–639. doi: 10.1152/jn.00626.2002. [DOI] [PubMed] [Google Scholar]
- Escudero M., Cheron G., Godaux E. Discharge properties of brain stem neurons projecting to the flocculus in the alert cat. II. Prepositus hypoglossal nucleus. J Neurophysiol. 1996 Sep;76(3):1775–1785. doi: 10.1152/jn.1996.76.3.1775. [DOI] [PubMed] [Google Scholar]
- Eskiizmirliler S., Forestier N., Tondu B., Darlot C. A model of the cerebellar pathways applied to the control of a single-joint robot arm actuated by McKibben artificial muscles. Biol Cybern. 2002 May;86(5):379–394. doi: 10.1007/s00422-001-0302-1. [DOI] [PubMed] [Google Scholar]
- Fujita M. Adaptive filter model of the cerebellum. Biol Cybern. 1982;45(3):195–206. doi: 10.1007/BF00336192. [DOI] [PubMed] [Google Scholar]
- Gibson Alan R., Horn Kris M., Pong Milton. Inhibitory control of olivary discharge. Ann N Y Acad Sci. 2002 Dec;978:219–231. doi: 10.1111/j.1749-6632.2002.tb07569.x. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Graf W., Simpson J. I., Leonard C. S. Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells. J Neurophysiol. 1988 Dec;60(6):2091–2121. doi: 10.1152/jn.1988.60.6.2091. [DOI] [PubMed] [Google Scholar]
- Hirata Y., Highstein S. M. Acute adaptation of the vestibuloocular reflex: signal processing by floccular and ventral parafloccular Purkinje cells. J Neurophysiol. 2001 May;85(5):2267–2288. doi: 10.1152/jn.2001.85.5.2267. [DOI] [PubMed] [Google Scholar]
- Holdefer R. N., Miller L. E., Chen L. L., Houk J. C. Functional connectivity between cerebellum and primary motor cortex in the awake monkey. J Neurophysiol. 2000 Jul;84(1):585–590. doi: 10.1152/jn.2000.84.1.585. [DOI] [PubMed] [Google Scholar]
- 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]
- Lisberger S. G., Fuchs A. F. Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement. J Neurophysiol. 1978 May;41(3):764–777. doi: 10.1152/jn.1978.41.3.764. [DOI] [PubMed] [Google Scholar]
- Markert G., Büttner U., Straube A., Boyle R. Neuronal activity in the flocculus of the alert monkey during sinusoidal optokinetic stimulation. Exp Brain Res. 1988;70(1):134–144. doi: 10.1007/BF00271855. [DOI] [PubMed] [Google Scholar]
- 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]
- 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]
- Miles F. A., Fuller J. H., Braitman D. J., Dow B. M. Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys. J Neurophysiol. 1980 May;43(5):1437–1476. doi: 10.1152/jn.1980.43.5.1437. [DOI] [PubMed] [Google Scholar]
- Nagao S. Eye velocity is not the major factor that determines mossy fiber responses of rabbit floccular Purkinje cells to head and screen oscillation. Exp Brain Res. 1990;80(1):221–224. doi: 10.1007/BF00228867. [DOI] [PubMed] [Google Scholar]
- 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]
- Nakao S., Curthoys I. S., Markham C. H. Eye movement related neurons in the cat pontine reticular formation: projection to the flocculus. Brain Res. 1980 Feb 10;183(2):291–299. doi: 10.1016/0006-8993(80)90465-5. [DOI] [PubMed] [Google Scholar]
- Nicolelis Miguel A. L. Brain-machine interfaces to restore motor function and probe neural circuits. Nat Rev Neurosci. 2003 May;4(5):417–422. doi: 10.1038/nrn1105. [DOI] [PubMed] [Google Scholar]
- Noda H., Suzuki D. A. Processing of eye movement signals in the flocculus of the monkey. J Physiol. 1979 Sep;294:349–364. doi: 10.1113/jphysiol.1979.sp012934. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Noda H., Warabi T., Ohno M. Response properties and visual receptive fields of climbing and mossy fibers terminating in the flocculus of the monkey. Exp Neurol. 1987 Feb;95(2):455–471. doi: 10.1016/0014-4886(87)90152-x. [DOI] [PubMed] [Google Scholar]
- 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]
- Quaia C., Lefèvre P., Optican L. M. Model of the control of saccades by superior colliculus and cerebellum. J Neurophysiol. 1999 Aug;82(2):999–1018. doi: 10.1152/jn.1999.82.2.999. [DOI] [PubMed] [Google Scholar]
- Ramnani N., Miall C. Expanding cerebellar horizons. Trends Cogn Sci. 2001 Apr 1;5(4):135–136. doi: 10.1016/s1364-6613(00)01635-1. [DOI] [PubMed] [Google Scholar]
- 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]
- Spoelstra J., Schweighofer N., Arbib M. A. Cerebellar learning of accurate predictive control for fast-reaching movements. Biol Cybern. 2000 Apr;82(4):321–333. doi: 10.1007/s004220050586. [DOI] [PubMed] [Google Scholar]
- Stone L. S., Lisberger S. G. Visual responses of Purkinje cells in the cerebellar flocculus during smooth-pursuit eye movements in monkeys. I. Simple spikes. J Neurophysiol. 1990 May;63(5):1241–1261. doi: 10.1152/jn.1990.63.5.1241. [DOI] [PubMed] [Google Scholar]
- Voogd J., Gerrits N. M., Ruigrok T. J. Organization of the vestibulocerebellum. Ann N Y Acad Sci. 1996 Jun 19;781:553–579. doi: 10.1111/j.1749-6632.1996.tb15728.x. [DOI] [PubMed] [Google Scholar]
- Yamamoto Kenji, Kobayashi Yasushi, Takemura Aya, Kawano Kenji, Kawato Mitsuo. Computational studies on acquisition and adaptation of ocular following responses based on cerebellar synaptic plasticity. J Neurophysiol. 2002 Mar;87(3):1554–1571. doi: 10.1152/jn.00166.2001. [DOI] [PubMed] [Google Scholar]
- 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]