Summary
Each Purkinje cell axon with its recurrent collaterals occupies a roughly triangular space in the folium, apex pointed towards the white matter and base against the Purkinje cell layer. The axon is smooth initially but develops distensions that become more obvious at twists and turns and at points where collaterals originate. These thin, finely beaded collaterals make characteristic acute angles with the axon from which they issue. The collaterals bifurcate further, their terminal branches becoming more varicose, intertwining with each other to form plexuses in the molecular and granular layers. These fiber plexuses are found in three locations: (1) the recurrent collateral plexus in the granular layer which synapses with dendrites and somata of deep Golgi II neurons; (2) the profuse infraganglionic plexus, boutons of which terminate in relation with the somata and dendrites of Purkinje cells and Lugaro cells, in addition to participating in other complex synaptic arrangements in the neuropil; (3) the sparse supraganglionic plexus which forms synapses with dendrites of Purkinje cells and occasionally with basket cells.
In electron micrographs, terminals belonging to recurrent collaterals contain a mixture of neurofilaments, microtubules, and slender mitochondria with a loose array of flat, elliptical, and round synaptic vesicles embedded in a dark filamentous matrix. It is usual to find a cluster of boutons on the postsynaptic surface. Each synapse consists of several separate macular junctional complexes. The synaptic cleft is widened and contains a dense fibrous material while both pre- and postsynaptic components have very shallow, symmetrical filamentous densities adherent to the cytoplasmic surfaces of the membranes.
It is suggested that recurrent collaterals from axons of Purkinje cells may provide a rapid monosynaptic feed-back mechanism for inhibitory control of Purkinje cell responses. These collaterals may also participate in a slower positive feed-forward circuit or resetting mechanism involving at least two synapses. The existence of this circuit is indicated by synapses on deep Golgi II neurons. The inhibition of Golgi II cells may depress their inhibitory activity on surrounding granule cells, thus resetting the mechanism for the subsequent responses to excitatory afferent input. Recurrent collateral inhibition also may aid in the disinhibition of Purkinje cells through the depression of basket cell activity.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Andres, K. H.: Über die Feinstruktur besonderer Einrichtungen in markhaltigen Nervenfasern des Kleinhirns der Ratte. Z. Zellforsch. 65, 701–712 (1965).
Cajal, S. R.: Estructura de los centros nerviosos de las aves. Rev. trimestr. Histol. Nos. 1, 2 (1888).
Cajal, S. R.: Sobre las fibras nerviosas de la capa granulosa del cerebelo. Rev. trimestr. Histol. No. 4 (1889).
Cajal, S. R.: Sur les fibres de la couche granuleuse du cervelet et sur l'évolution des éléments cérébelleux. Int. Mschr. Anat. Physiol. 7 (1890).
—: Histologie du système nerveux de l'homme et des vertébrés, T. II. Trad. par L. Azoulay. Paris: Maloine 1911.
—: Sobre ciertos plexos pericelulares de la capa de los granos del cerebelo. Trab. Lab. Invest. biol. Madrid 10, 273–276 (1912).
—, Illera, R.: Quelques nouveaux détails sur la structure de l'écorce cérébelleuse. Trav. Lab. Recher. biol. 1, 2 (1907).
Chan-Palay, V., Palay, S. L.: Interrelations of basket cell axons and climbing fibers in the cerebellar cortex of rat. Z. Anat. Entwickl.-Gesch. 132, 191–227 (1970).
——: Tendril and glomerular collaterals of climbing fibers in the granular layer of the rat's cerebellar cortex. Z. Anat. Entwickl.-Gesch. (1971a) 133, 247–273 (1971).
——: The synapse en marron between Golgi II neurons and mossy fibers in the rat's cerebellar cortex. Z. Anat. Entwickl.-Gesch. (1971b) 133 274–289 (1971).
Eccles, J., Ito, M., Szentágothai, J.: The cerebellum as neuronal machine. Berlin-Heidelberg-New York: Springer 1967.
—, Llinás, R., Sasaki, K.: The action of antidromic impulses on the cerebellar Purkinje cells J. Physiol. (Lond.) 182, 315–345 (1966).
Fox, C. A.: The intermediate cells of Lugaro in the cerebellar cortex of monkey. J. comp. Neurol. 112, 39–51 (1959).
—, Bertram, E. G.: Connections of the Golgi cells and the intermediate cells of Lugaro in the cerebellar cortex of the monkey (Abstract). Anat. Rec. 118, 423–424 (1954).
Fox, C. A., Hillman, D. E., Siegesmund, K. A., Dutta, C. R.: The primate cerebellar cortex: A Golgi and electron microscopic study. In: The cerebellum (C. A. Fox and R. S. Snider, eds.). Progr. Brain Res. 25, 174–225 (1967).
Golgi, C.: Sulla fina anatomia del cervelletto umano (1874). In: Opera omnia, vol. I: Istologia normale, 1870–1883, Milano: Ulrico Hoepli 1903.
Gray, E. G.: Axo-somatic and axo-dendritic synapses of the cerebral cortex: An electron microscope study. J. Anat. (Lond.) 93, 420–433 (1959).
Hámori, J., Szentágothai, J.: Identification of synapses formed in the cerebellar cortex by Purkinje axon collaterals: an electron microscopic study. Exp. Brain Res. 15, 118–128 (1968).
Jakob, A.: Das Kleinhirn. In: Handbuch der mikroskopischen Anatomie des Menschen, hrsg. von W. vonMöllendorff, Bd. IV, Teil 1, S. 779–784. Berlin: Springer 1928.
Jansen, J., Brodal, A.: Das Kleinhirn. In: Handbuch der mikroskopischen Anatomie des Menschen, hrsg. von W. Bargmann, Bd. IV, Teil 8 (Ergänzung zu Bd. IV, Teil 1), S. 101–103. Berlin-Göttingen-Heidelberg: Springer 1958.
Kaiserman-Abramof, I. R., Palay, S. L.: Fine structural studies of the cerebellar cortex in a mormyrid fish. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 171–204. Chicago: AMA-ERF Institute for Biomedical Research 1969.
Kölliker, A.: Handbuch der Gewebelehre des Menschen, Bd. II: Nervensystem, S. 349–350. Leipzig: Wilhelm-Engelmann 1896.
Larramendi, L. M. H., Lemkey-Johnston, N. J.: The distribution of recurrent Purkinje collateral synapses in the mouse cerebellar cortex: An electron microscopic study. J. comp. Neurol. 138, 451–482 (1970).
—, Victor, T.: Synapses on the Purkinje cell spines in the mouse. An electronmicroscopic study. Brain Res. 5, 15–30 (1967).
Larsell, O.: The morphogenesis and adult pattern of the lobules and fissures of the cerebellum of the white rat. J. comp. Neurol. 97, 281–356 (1952).
Lemkey-Johnston, N. J., Larramendi, L. M. H.: Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum. J. comp. Neurol. 134, 73–112 (1968).
Llinás, R., Ayala, J. S.: Purkinje axon collateral action upon interneurons in the cerebellar cortex. In: Symposium on neurophysiological basis of normal and abnormal motor activities, Parkinson's Disease-Information and Research Center (M. D. Yahr and D. P. Purpura, eds.). Hewlett, N. Y.: Haven Press 1967.
Nieuwenhuys, R., Nicholson, C.: Aspects of the histology of the cerebellum of mormyrid fishes. In: Neurobiology of cerebellar evolution and development (R. Llinás, ed.), p. 135–169. Chicago: AMA-ERF Institute for Biomedical Research 1969.
O'Leary, J. L., Petty, J., Smith, J. M., O'Leary, M., Inukai, J.: Cerebellar cortex of rat and other animals. A structural and ultrastructural study. J. comp. Neurol. 134, 401–432 (1968).
Retzius, G.: Biologische Untersuchungen. Neue Folge III. Stockholm: Samson & Wallin 1892.
Valverde, F.: The Golgi method. A tool for comparative structural analysis. In: Contemporary research methods in neuroanatomy (W. J. H. Nauta and S. O. E. Ebbesson, eds.), p. 12–31. Berlin-Heidelberg-New York: Springer 1970.
Author information
Authors and Affiliations
Additional information
Supported by U.S. Public Health Service Research Grant NS03659 and Training Grant NS05591 from the National Institute of Neurological Diseases and Stroke.
Rights and permissions
About this article
Cite this article
Chan-Palay, V. The recurrent collaterals of Purkinje cell axons: A correlated study of the rat's cerebellar cortex with electron microscopy and the Golgi method. Z. Anat. Entwickl. Gesch. 134, 200–234 (1971). https://doi.org/10.1007/BF00519300
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00519300