Hostname: page-component-78c5997874-g7gxr Total loading time: 0 Render date: 2024-11-10T05:48:07.917Z Has data issue: false hasContentIssue false

Integrative Versus Delay Line Characteristics of Cerebellar Cortex

Published online by Cambridge University Press:  18 September 2015

W.A. MacKay
Affiliation:
Department of Physiology, University of Toronto, Toronto, Canada
J.T. Murphy*
Affiliation:
Department of Physiology, University of Toronto, Toronto, Canada
*
Department of Physiology, Medical Sciences Building, University of Toronto, Toronto, Ont. M5S 1A8, Canada
Rights & Permissions [Opens in a new window]

Summary:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

In order to determine which of two general models (“tapped delay line” or “integrator”) provides a more accurate description of mammalian Purkinje cell (P-cell) activation by natural stimulation, the spatial and temporal characteristics of a population of neurons in cerebellar cortex responsive to small controlled stretches of forelimb muscles were examined in awake, locally anesthetized cats. Stretch of a single wrist muscle excited P-cells over a distance of about 1 mm in the long axis of a folium, a span which is at most half the length of parallel fibers. Both granule cells and molecular layer interneurons were excited over a wider zone than P-cells.

Furthermore, P-cells across a response zone all fired on the average at the same time, as determined by computing peristimulus cross-interval histograms from pairs of simultaneously recorded neurons. Consistent delays could only be demonstrated in the minimal response latencies as measured from peristimulus time histograms. These delays, however, were longer than could be ascribed to parallel fiber conduction velocity.

No evidence, therefore, was found in cat cerebellum to support the “tapped delay line” model, which postulates the successive activation of P-cells as an excitatory volley travels along a parallel fiber beam. Instead, an integrative mode of operation seems to predominate: a relatively wide substratum of activated granule cells simultaneously activates a narrower focus of P-cells centrally situated with respect to the granule cell population. The role of inhibitory interneurons in promoting the “integrator” model is discussed.

Type
Research Article
Copyright
Copyright © Canadian Neurological Sciences Federation 1976

References

REFERENCES

Allen, G. I., Azzena, G. B. and Ohno, T. (1974). Somatotopically organized inputs from fore- and hindlimb areas of sensorimotor cortex to cerebellar Purkyne cells. Experimental Brain Research, 20, 255272.Google ScholarPubMed
Armstrong, D. M., Harvey, R. J. and Schild, R. F. (1973). The spatial organization of climbing fibre branching in the cat cerebellum. Experimental Brain Research, 18, 4058.CrossRefGoogle ScholarPubMed
Bell, C. C. and Grimm, R. J. (1969). Discharge properties of Purkinje cells recorded on single and double microelectrodes. Journal of Neurophysiology, 32, 10441055.CrossRefGoogle ScholarPubMed
Blake, R. C. (1974). Weighted averaging simplifies curve fitting. Electronics, 47 (5), 136138.Google Scholar
Bloedel, J. R. (1975). Cerebellar afferent systems: a review. Progress in Neurobiology, 2, 168.CrossRefGoogle Scholar
Braitenberg, V. (1961). Functional interpretation of cerebellar histology. Nature, 190, 539540.CrossRefGoogle Scholar
Brand, S., Dahl, A. and Mugnaini, E. (1974). Length of parallel fibers in the cat cerebellar cortex. Anatomical Record, 178, 315.Google Scholar
Cooke, J. D., Larson, B., Oscarsson, O. and Sjölund, B. (1971). Organization of afferent connections to cuneocerebellar tract. Experimental Brain Research, 13, 359377.CrossRefGoogle ScholarPubMed
Courville, J., Faraco-Cantin, F. and Diakiw, N. (1974). A functionally important feature of the distribution of the olivo-cerebellar climbing fibers. Canadian Journal of Physiology and Pharmacology, 52, 12121217.CrossRefGoogle ScholarPubMed
Eccles, J.C, Faber, D., Murphy, J. and Sabah, N. and Töboříkoví, H. (1971a). Afferent volleys in limb nerves influencing impulse discharges in cerebellar cortex. I. In mossy fibers and granule cells. Experimental Brain Research, 13, 1535.CrossRefGoogle ScholarPubMed
Eccles, J. C, Faber, D.. Jviurphy, J., Sabah, N. and Töboříkoví, H. (1971b). Afferent volleys in limb nerves influencing impulse discharges in cerebellar cortex. II. In Purkyne cells. Experimental Brain Research, 13, 3653.CrossRefGoogle Scholar
Eccles, J. C, Faber, D.M., Urphy, J., Sabah, N. and Töboříkoví, H. (1971c). Investigations on integration of mossy fiber inputs to Purkyne cells in the anterior lobe. Experimental Brain Research, 13, 5477.CrossRefGoogle ScholarPubMed
Eccles, J.C, Ito, M. and Szentágothai, J. (1967). “The Cerebellum as a Neuronal Machine.New York, Springer.CrossRefGoogle Scholar
Eccles, J. ç., Sabah, N., Schmidt, R. and Töboříkoví, H. (1972). Integration by Purkyne cells of mossy and climbing fiber inputs from cutaneous mechanorecep-tors. Experimental Brain Research, 15, 498520.CrossRefGoogle Scholar
Ekerot, C. F. and Larson, B. (1972). Differential termination of the exteroceptive and proprioceptive components of the cuneocerebellar tract. Brain Research, 36, 420424.CrossRefGoogle ScholarPubMed
Ekerot, C. F. and Larson, B. (1973). Correlation between sagittal projection zones of climbing and mossy fibre paths in cerebellar anterior lobe. Brain Research, 64, 446450.CrossRefGoogle ScholarPubMed
Fox, C. A. and Barnard, J. W. (1957). A quantitative study of the Purkinje cell de-ndritic branchlets and their relationship to afferent fibres. Journal of Anatomy, 91, 299313.Google ScholarPubMed
Freeman, J. A. (1969). The cerebellum as a timing device: an experimental study in the frog. In: Neurobiology of Cerebellar Evolution and Development, edited by Llinas, R., American Medical Association: Chicago, pp. 397420.Google Scholar
Freeman, J. A. (1970). Responses of cat cerebellar Purkinje cells to convergent in-puts from cerebral cortex and peripheral sensory systems. Journal of Neurophysiology, 33, 697712.CrossRefGoogle Scholar
Freeman, J. A. and Nicholson, C. N. (1970). Space-time transformation in the frog cerebellum through an intrinsic tapped delay-line. Nature, 226, 640642.Google ScholarPubMed
Gardner-Medwin, A.R. (1972). An extreme supernormal period in cerebellar parallel fibres. Journal of Physiology, 222, 357371.CrossRefGoogle ScholarPubMed
Gerstein, G. L. and Perkel, D. H. (1972). Mutual temporal relationships among neuronal spike trains. Statistical techniques for display and analysis. Biophysical Journal, 12, 453473.CrossRefGoogle ScholarPubMed
Houk, J. C. and Walsh, J. V. (1971). The length and organization of parallel fibres. International Congress of Physiological Sciences, Proceedings, p. 263.Google Scholar
Kemali, M. and Braitenberg, V. (1969). Atlas of the frog’s brain. New York, Springer- Verlag.Google Scholar
Kornhuber, H. H. (1971). Motor functions of cerebellum and basal ganglia: The cerebellocortical saccadic (ballistic) clock, the cerebellonuclear hold regulator, and the basal ganglia ramp (voluntary speed smooth movement) generator. Kybernetik, 8, 157162.CrossRefGoogle ScholarPubMed
Kwan, H.C. and Murphy, J.T. (1974). Extracellular current density analysis of responses in cerebellar cortex to mossy fiber activation. Journal of Neurophysiology, 37, 947953.CrossRefGoogle ScholarPubMed
Lange, W. (1975). Cell number and cell density in the cerebellar cortex of man and some other mammals. Cell Tissue Research, 157, 115124.CrossRefGoogle ScholarPubMed
Llinís, R. and Hillman, D.E. (1969). Physiological and morphological organization of the cerebellar circuits in various vertebrates. In: Neurobiology of Cerebellar Evolution and Development, edited by Llinas, R., American Medical Association: Chicago, pp. 4373.Google Scholar
Llinís, R. and Nicholson, C. (1971). Electrophysiological properties of dendrites and somata in alligator Purkinje cells. Journal of Neurophysiology, 34, 532551.CrossRefGoogle Scholar
MacKay, W.A. and Murphy, J.T. (1973). Profile of a simple cerebellar cortical response zone. Canada Physiology, 4, p. 41.Google Scholar
MacKay, W.A. and Murphy, J.T. (1974). Responses of interpositus neurons to passive muscle stretch. Journal of Neurophysiology, 37, 14101423.CrossRefGoogle ScholarPubMed
MacKay, W.A. and Murphy, J.T. (1975). A mechanism for cerebellar integration. Canadian Federation of Biological Societies, Proceedings, 18, p. 148.Google Scholar
Mugnaini, E., Atluri, R.L. and Houk, J. C. (1974). Fine structure of granular layer in turtle cerebellum with emphasis on large glomeruli. Journal of Neurophysiology, 37, 129.CrossRefGoogle ScholarPubMed
Murphy, J.T., Kwan, H., MacKay, W. A. and Wong, Y.C. (1974). Evaluation of neuronal spike trains in neurophysiological experiments. Physiology and Behavior, 13, 313315.CrossRefGoogle ScholarPubMed
Murphy, J.T., MacKay, W.A. and Johnson, F. (1973). Differences between cerebellar mossy and climbing fibre responses to natural stimulation of forelimb muscle proprioceptors. Brain Research, 55, 263289.CrossRefGoogle ScholarPubMed
Nicholson, C. Llinas, R. and Precht, W. (1969). Neural elements of the cerebellum in elasmobranch fishes: structural and functional characteristics. In: Neurobiology of Cerebellar Evolution and Development, edited by Llinas, R., American Medical Association: Chicago, pp. 215243.Google Scholar
Oscarsson, O. (1973). Functional organization of spinocerebellar paths. In: Hand-book of Sensory Physiology, vol. 2, Somatosensory System, edited by Iggo, A.. Springer: New York, pp. 339380.Google Scholar
Palkovits, M., Magyar, P. and Szentagothai, J. (1971). Quantitative histological analysis of the cerebellar cortex in the cat. III. Structural organization of the molecular layer. Brain Research, 34, 118.CrossRefGoogle Scholar
Perkel, D., Gerstein, G. and Moore, G. (1967). Neuronal spike trains and stochastic point processes. II. Simultaneous spike trains. Biophysical Journal, 7, 419440.CrossRefGoogle ScholarPubMed
Precht, W. and Llinas, R. (1969). Functional organization of the vestibular affer-ents to the cerebellar cortex of frog and cat. Experimental Brain Research, 9, 3052.CrossRefGoogle Scholar
Rosen, I. and Sjòlund, B. (1973). Organization of group 1 activated cells in the main and external cunçate nuclei of the cat: convergence patterns demonstrated by natural stimulation. Experimental Brain Research, 16, 238246.Google Scholar
Sabah, N.H. and Murphy, J.T. (1971).A superposition model of the spontaneous synaptic excitation of cerebellar Purkinje cells. Biophysical Journal, 11, 414428.CrossRefGoogle Scholar
Szentágothai, J. (1968). Structuro-functional considerations of the cerebellar neuron network. Institute of Electrical and Electronic Engineers, Proceedings. 56, 960968.CrossRefGoogle Scholar
Walsh, J.V., Houk, J.C. and Mugnaini, E. (1974). Identification of unitary potentials in turtle cerebellum and correlations with structures in granular layer. Journal of Neurophysiology, 37, 3047.CrossRefGoogle ScholarPubMed
Voogd, J. (1969). The importance of fiber connections in the comparative anatomy of the mammalian cerebellum. In: Neurobiology of Cerebellar Evolution and Develop-ment, edited by Llinas, R., American Medical Association: Chicago, pp. 493514.Google Scholar