Physiological and anatomical studies of the interactions between Purkinje cells and basket cells in the cat's cerebellar cortex: evidence for a unitary relationship

Intracellular recordings have been obtained from neurons in lobule V of the cat's vermis, which were identified as basket cells following intracellular injections of HRP. Stimulation of the inferior cerebellar peduncle or peripheral nerves elicited an initial depolarizing and subsequent hyperpolarizing response. Neither potential could be graded with changes in stimulus intensity; both displayed all-or-none properties at threshold levels of stimulation. The depolarization and hyperpolarization were confirmed as an excitatory postsynaptic potential and an inhibitory postsynaptic potential (IPSP), respectively, on the basis of their response to intracellular injections of hyperpolarizing and depolarizing currents into the cell body. A possible source of the unitary IPSP is the Purkinje cell, via its recurrent axonal collaterals. To test this hypothesis, an electron microscopic analysis was carried out to define the synaptic relationships between the recurrent collaterals of an HRP-filled Purkinje cell and 3 basket cells. Serial section analysis reveals that collaterals from a single Purkinje cell contact several basket cells, but each basket cell received somatic input from only one Purkinje cell. These data provide an anatomical substrate for the unitary IPSP observed during intracellular recording from basket cells. The unitary nature of the Purkinje cell-basket cell interaction indicates that a very limited population of cortical neurons may be involved in local circuits that integrate afferent information in the cerebellar cortex.

[1]  D. Harriman CEREBELLAR CORTEX, CYTOLOGY AND ORGANIZATION , 1974 .

[2]  Professor Dr. John C. Eccles,et al.  The Cerebellum as a Neuronal Machine , 1967, Springer Berlin Heidelberg.

[3]  T. Ebner,et al.  Increased responsiveness of Purkinje cells associated with climbing fiber inputs to neighboring neurons. , 1983, Journal of neurophysiology.

[4]  G. Bishop Quantitative analysis of the recurrent collaterals derived from Purkinje cells in zone X of the cat's vermis , 1988, The Journal of comparative neurology.

[5]  J. Bloedel,et al.  Functional relationship among neurons of the cerebellar cortex in the absence of anesthesia. , 1969, Journal of neurophysiology.

[6]  T. Ebner,et al.  Temporal patterning in simple spike discharge of Purkinje cells and its relationship to climbing fiber activity. , 1981, Journal of neurophysiology.

[7]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. , 1980, The Journal of physiology.

[8]  O. Oscarsson Functional units of the cerebellum - sagittal zones and microzones , 1979, Trends in Neurosciences.

[9]  R. S. Gregory,et al.  Action of interneurons and axon collaterals in cerebellar cortex of a primate. , 1972, Journal of neurophysiology.

[10]  J. Desclin,et al.  The olivocerebellar system. I. Delayed and slow inhibitory effects: An overlooked salient feature of cerebellar climbing fibers , 1980, Brain Research.

[11]  G. Bishop,et al.  Heterogeneity in the pattern of distribution of the axonal collaterals of Purkinje cells in zone b of the cat's vermis: An intracellular HRP study , 1986, The Journal of comparative neurology.

[12]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[13]  Masao Ito The Cerebellum And Neural Control , 1984 .

[14]  R. Llinás,et al.  Cytology and organization of rat cerebellar organ cultures , 1988, Neuroscience.

[15]  G. Bishop,et al.  The pattern of distribution of the local axonal collaterals of Purkinje cells in the intermediate cortex of the anterior lobe and paramedian lobule of the cat cerebellum , 1982, The Journal of comparative neurology.

[16]  T J Ebner,et al.  Correlation between activity of Purkinje cells and its modification by natural peripheral stimuli. , 1981, Journal of neurophysiology.

[17]  N. Lemkey-Johnston,et al.  Types and distribution of synapses upon basket and stellate cells of the mouse cerebellum: An electron microscopic study , 1968, The Journal of comparative neurology.

[18]  C. G. Phillips,et al.  Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats , 1956, The Journal of physiology.

[19]  H. Nauta Tracing neural connections with horseradish peroxidase M. M. Mesulam (Ed.). John Wiley, Chichester (1982). 280 pp., Cloth, $52.00/£22.00; paper, $26.00/£11.00 , 1982, Neuroscience.

[20]  G. Bishop,et al.  The synaptic features of horseradish peroxidase-labelled recurrent collaterals in the ganglionic plexus of the cat cerebeliar cortex , 1982, Journal of neurocytology.

[21]  S. Palay,et al.  Cerebellar Cortex: Cytology and Organization , 1974 .

[22]  G. Bishop,et al.  An analysis of the morphology and cytology of HRP labeled Purkinje cells , 1980, Brain Research Bulletin.

[23]  D E Hillman,et al.  The primate cerebellar cortex: a Golgi and electron microscopic study. , 1967, Progress in brain research.