Skip to main content

A Theory of Cerebellar Cortex

  • Chapter
Book cover From the Retina to the Neocortex

Summary

  1. 1.

    A detailed theory of cerebellar cortex is proposed whose consequence is that the cerebellum learns to perform motor skills. Two forms of input-output relation are described, both consistent with the cortical theory. One is suitable for learning movements (actions), and the other for learning to maintain posture and balance (maintenance reflexes).

  2. 2.

    It is known that the cells of the inferior olive and the cerebellar Purkinje cells have a special one-to-one relationship induced by the climbing fibre input. For learning actions, it is assumed that:

    1. (a)

      each olivary cell responds to a cerebral instruction for an elemental movement. Any action has a defining representation in terms of elemental movements, and this representation has a neural expression as a sequence of firing patterns in the inferior olive; and

    2. (b)

      in the correct state of the nervous system, a Purkinje cell can initiate the elemental movement to which its corresponding olivary cell responds.

  3. 3.

    Whenever an olivary cell fires, it sends an impulse (via the climbing fibre input) to its corresponding Purkinje cell. This Purkinje cell is also exposed (via the mossy fibre input) to information about the context in which its olivary cell fired; and it is shown how, during rehearsal of an action, each Purkinje cell can learn to recognize such contexts. Later, when the action has been learnt, occurrence of the context alone is enough to fire the Purkinje cell, which then causes the next elemental movement. The action thus progresses as it did during rehearsal.

  4. 4.

    It is shown that an interpretation of cerebellar cortex as a structure which allows each Purkinje cell to learn a number of contexts is consistent both with the distributions of the various types of cell, and with their known excitatory or inhibitory natures. It is demonstrated that the mossy fibre-granule cell arrangement provides the required pattern discrimination capability.

  5. 5.

    The following predictions are made.

    1. (a)

      The synapses from parallel fibres to Purkinje cells are facilitated by the conjunction of presynaptic and climbing fibre (or post-synaptic) activity. Reprinted with permission of The Physiological Society, Oxford, England.

    2. (b)

      No other cerebellar synapses are modifiable.

    3. (c)

      Golgi cells are driven by the greater of the inputs from their upper and lower dendritic fields.

  6. 6.

    For learning maintenance reflexes, 2(a) and 2 (b) are replaced by 2’. Each olivary cell is stimulated by one or more receptors, all of whose activities are usually reduced by the results of stimulating the corresponding Purkinje cell.

  7. 7.

    It is shown that if (2’) is satisfied, the circuit receptor → olivary cell → Purkinje cell → effector may be regarded as a stabilizing reflex circuit which is activated by learned mossy fibre inputs. This type of reflex has been called a learned conditional reflex, and it is shown how such reflexes can solve problems of maintaining posture and balance.

  8. 8.

    5(a), and either (2) or (2’) are essential to the theory: 5(b) and 5(c) are not absolutely essential, and parts of the theory could survive the disproof of either.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Armstrong, D. M., Eccles, J. C., Harvey, R. J., Matthews, P. B. C. (1968). Responses in the dorsal accessory olive of the cat to stimulation of hind limb afferents. J. Physiol. 194, 125–145.

    Google Scholar 

  • Brlndley, G. S. (1964). The use made by the cerebellum of the information that it receives from sense organs. Int. Brain. Res. Org. Bulletin 3, 80.

    Google Scholar 

  • Brindley, G. S. (1969). Nerve net models of plausible size that will perform many of very many simple learning task. Proc. R. Soc. B. (In the Press.)

    Google Scholar 

  • Brodal, A. (1954). Afferent cerebellar connections. In Aspects of Cerebellar Anatomy, ed. JANSEN, J. and BRODAL, A. ch. II, pp. 82–188.

    Google Scholar 

  • Oslo: Johan Grundt Tanum Forlag. Cajal, R. Y. (1911). Histologie du Systeme Nerveux,Tome II, 1955 edn., p. 57, C.S.I.C.: Madrid.

    Google Scholar 

  • Eccles, J. C., Ito, M. and Szentaoothai, J. (1967). The Cerebellum as a Neuronal Machine. Berlin: Springer-Verlag.

    Google Scholar 

  • Escobar, A., Sampedro, E. D. and Dow, R. S. (1968). Quantitative data on the inferior olivary nucleus in man, cat and vampire bat. J. comp. Neurcl. 132, 397–403.

    Google Scholar 

  • Hebb, D. O. (1949). The Organization of Behaviour, p. 62. New York: Wiley.

    Google Scholar 

  • Uhr, L. and Vossler, C. (1961). A pattern recognition program that generates, evaluates and adjusts its own operators. Proc. west. jt. Computer Conf. 19, 555–569.

    Google Scholar 

  • Walbero, F. (1954). Descending connections to the inferior olive. In Aspects of Cerebellar Anatomy, ed. Jansen, J. and Brodal, A., ch. iv, pp. 249–263. Oslo: Johan Grundt Tanum Forlag.

    Google Scholar 

  • Albus JS (1971): A theory of cerebellar function. Math Biosci 10: 25–61

    Article  Google Scholar 

  • Andersson G, Armstrong DM (1987): Complex spikes in Purkinje cells in the lateral vermis (b zone) of the cat cerebellum during locomotion. J Physiol 385: 107–134

    Google Scholar 

  • Armstrong DM, Edgley SA, Lidierth M (1988): Complex spikes in Purkinje cells of the paravermal part of the anterior lobe of the cat cerebellum during locomotion. J Physiol 400: 405–414

    Google Scholar 

  • Brindley GS (1964): The use made by the cerebellum of the information that it receives from the sense organs. IBRO Bull 3 (3): 80

    Google Scholar 

  • Cuenod M, Do KQ, Vollenweider F, Streit P (1988): Cerebellar climbing fibers: excitatory amino acid and adensoine release. Neurobiology of the Cerebellar Systems: A Centenary of Ramón y Cajal’s Description of the Cerebellar Circuits. p. 26 (Abstr.)

    Google Scholar 

  • Ebner TJ, Bloedel JR (1981): Role of climbing fiber afferent input in determining responsiveness of Purkinje cells to mossy fiber inputs. J Neurophysiol 45: 962–971

    Google Scholar 

  • Ebner TJ, Yu QX, Bloedel JR (1983): Increase in Purkinje cell gain associated with naturally activated climbing fiber input. J Neurophysiol 50: 205–219

    Google Scholar 

  • Eccles JC, Ito M, Szentagothai J (1967): The cerebellum as a neuronal machine. New York: Springer-Verlag, Inc

    Google Scholar 

  • Ekerot CF (1985): Climbing fiber actions of Purkinje cells—plateau potentials and long-lasting depression of parallel fiber responses. In: Cerebellar Functions Bloedel JR, Dichgans J, Precht W, ed. New York: Springer-Verlag

    Google Scholar 

  • Ekerot C-F, Kano M (1985): Long-term depression of parallel fibre synapses following stimulation of climbing fibres. Brain Res 342: 357–360

    Article  Google Scholar 

  • Gerrits NM, Voogd J (1989): The topograhical organization of climbing and mossy fiber afferents in the flocculus and the ventral paraflocculus in rabbit, cat and monkey. Exp Brain Res Series 17: 26–29

    Google Scholar 

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

    Google Scholar 

  • Gilbert PFC (1974): A theory of memory that explains the function and structure of the cerebellum. Brain Res 70: 1–18

    Article  Google Scholar 

  • Gilbert PFC, Thach WT (1977): Purkinje cell activity during motor learning. Brain Res 128: 309–328

    Article  Google Scholar 

  • Gonshor A, Melvill-Jones G (1976): Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol Lond 256: 381–414

    Google Scholar 

  • Harvey JA, Welch JP (1988): Cerebellar regulation of the conditioned and unconditioned nicitating membrane reflex: analysis of sensory, associative and motor functions after reversible and irreversible cerebellar lesions. Neurobiology of the Cerebellar Systems: A Centenary of Ramón y Cajal’s Description of the Cerebellar Circuits. p. 36 (abstr.)

    Google Scholar 

  • Ito M (1972): Neural design of the cerebellar control system. Brain Res 40: 81–84

    Article  Google Scholar 

  • Ito M, Sakurai M, Tongroach P (1982): Climbing fibre induced depression of both mossy fiber responsiveness and glutamate sensitivity of cerebellar Purkinje cells. J Physiol Lond 324: 113–134

    Google Scholar 

  • Ito M, Shiida TN, Yamamoto M (1974): The cerebellar modification of rabbit’s horizontal vestibulo-ocular reflexin induced by sustained head rotation combined with visual stimulation. Proc Japan Acad 50: 85–89

    Google Scholar 

  • Kano M, Kato M (1987): Quisqualate receptors are specifically involved in cerebellar synaptic plasticity. Nature 325: 276–279

    Article  Google Scholar 

  • Leaton RN, Supple WF, Jr. (1986): Cerebellar vermis: essential for long-term habituation of the acoustic startle response. Science 232: 513–515

    Article  Google Scholar 

  • Llinas R (1970): Neuronal operations in cerebellar transactions. In: The Neurosciences: Second Study Program. Schnitt FO, ed. New York: Rockefeller University Press, pp 409–426

    Google Scholar 

  • Llinas R (1981): Electrophysiology of cerebellar networks. In: Handbook of Physiology, Section 1, Volume II, Part 2. Brooks, VB ed. pp 831–876

    Google Scholar 

  • Llinas R, Hess R (1976): Tetrodotoxin-resistant spikes in avian Purkinje cells. Proc Nat Acad Sci 73: 2520–2523

    Article  Google Scholar 

  • Llinas R, Nicholson C (1971): Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol 34: 532–551

    Google Scholar 

  • Llinas R, Sugimori M (1980a): Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305: 171–195

    Google Scholar 

  • Llinas R, Sugimori M (1980b): Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol 305: 197–213

    Google Scholar 

  • Llinas R, Volkind RA (1973): The olivocerebellar system: functional properties as revealed by harmaline-induced tremor. Exp Brain Res 18: 69–87

    Article  Google Scholar 

  • Llinas R, Walton K, Hillman DE, Sotelo C (1975): Inferior olive: its role in motor learning. Science 190: 1230–1231

    Article  Google Scholar 

  • Lisberger SG (1988): The neural basis for learning of simple motor skills. Science 242: 728–735

    Article  Google Scholar 

  • Luciani, L (1911–1924): Human Physiology. Welby FA, trans. London: MacMillan and Co., Ltd

    Google Scholar 

  • Marr D (1969): A theory of cerebellar cortex. J Physiol 202: 437–470

    Google Scholar 

  • McCormick DA, Thompson RF (1984): Cerebellum: essential involvement in the classically conditioned eyelid response. Science 223: 296–299

    Article  Google Scholar 

  • Miles FA, Fuller JRH, Braitman DJ, Dow BM (1980): Long-term adaptive changes in primate vestibulo-ocular reflexes III. Electro-physiological observations in flocculus of adapted monkeys. J Neurophysiol 43: 1437–1476

    Google Scholar 

  • Optican LM, Robinson DA (1980): Cerebellar-dependent adaptive control of primate saccadic system. J Neurophysiol 44: 1058–1080

    Google Scholar 

  • Rawson NR (1932): The story of the cerebellum. Canad MAT. 26: 220–225

    Google Scholar 

  • Rawson JA, Tilokskulchai K (1982): Climbing modification of cerebellar Purkinje cell responses to parallel fiber inputs. Brain Res 237: 492–497

    Article  Google Scholar 

  • Robinson DA (1976): Adaptive gain control of the vestibulo-ocular reflex by the cerebellum. J Neurophysiol 39: 954–969

    Google Scholar 

  • Simpson JI, Alley KE (1974): Visual climbing fiber input to rabbit vestibulo-cerebellum: a source of direction-specific information. Brain Res 82: 302–308

    Article  Google Scholar 

  • Thach WT (1980): Complex spikes, the inferior olive, and natural behavior. In: The Inferior Olivary Nucleus. Courville J, ed. New York: Raven, pp 349–360

    Google Scholar 

  • Watanabe E (1984): Neuronal events correlated with long-term adaptation of the horizontal vestibulo-ocular reflex in the primate flocculus. Brain Res 297: 169–174

    Article  Google Scholar 

  • Yeo CH, Hardiman MJ, Glickstein M (1984): Discrete lesions of the cerebellar cortex abolish classically conditioned nictitating membrane response of the rabbit. Behav Brain Res 13: 261–266

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1991 Birkhäuser Boston

About this chapter

Cite this chapter

Marr, D., Thach, W.T. (1991). A Theory of Cerebellar Cortex. In: Vaina, L. (eds) From the Retina to the Neocortex. Birkhäuser Boston. https://doi.org/10.1007/978-1-4684-6775-8_3

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-6775-8_3

  • Publisher Name: Birkhäuser Boston

  • Print ISBN: 978-1-4684-6777-2

  • Online ISBN: 978-1-4684-6775-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics