Electrophysiological study of the corticonuclear projection in the cat cerebellum

Experiments were designed to examine the relationship between the responses of Purkinje cells to natural peripheral stimuli and the location of these neurons within identified zones of the corticonuclear projection in lobule V of the cat cerebellar cortex. It was hypothesized that the corticonuclear zones are sharply demarcated and that the responses of Purkinje cells to a restricted natural stimulus is not localized to only one zone but rather is present and varies in character across these 3 zones. Initially the spatial distribution of the antidromic field potential evoked by stimulating in the fastigial (FN), lateral vestibular (LVN), and anterior interposed nuclei (AIN) was determined in sublobules Va-Vc in unanesthetized decerebrate cats. In some animals the corticonuclear projection was further examined by evaluating the location of Purkinje cells responding antidromically to stimuli in the FN, LVN and AIN, or FN, AIN and the posterior interposed nuclei (PIN). Once a Purkinje cell was identified, its simple and complex spike responses to a step-like flexion-extension passive movement of the ipsilateral forepaw were determined. The boundary based on the antidromic activation of Purkinje cells between the fastigial zone (FZ) and the anterior interposed zone (AIZ) in sublobules Va-Vc of the cerebellar cortex was highly reproducible from cat to cat, although there was a slight overlap between these zones based on the antidromic field potential. The FZ-AIZ border was located at 2.1 +/- 0.12 mm lateral and parallel to the midline. The FZ also contained a few cells projecting to the LVN. However, the AIZ only contained neurons projecting to the AIN. The boundary between AIZ and PIZ in lobule Va-Vc was between 3.3 and 3.8 mm from the midline and ran parallel to it. The peristimulus time histograms (PSTHs) of the simple and complex spike activity to a passive forepaw displacement revealed extensive modulation of neurons located across the mediolateral extent of the AI and PIZ. Both the simple and complex spike discharge of Purkinje cells projecting to the FN also were modulated, but to a lesser degree than cells in AIZ or PIZ. The spatial distribution of simple and complex spike responses recorded from Purkinje cells overlapped extensively. The data support previous findings that the corticonuclear projection is organized into longitudinally oriented sagittal zones. Electrophysiologically the boundaries were remarkably reproducible from animal to animal. The results also show that information processing involving the modulation of Purkinje cell activity in response to the forepaw stimulus occurs in all 3 zones examined.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  C. Bell,et al.  Relations among climbing fiber responses of nearby Purkinje Cells. , 1972, Journal of neurophysiology.

[2]  W. Chambers,et al.  Functional localization in the cerebellum. II. Somatotopic organization in cortex and nuclei. , 1955, A.M.A. archives of neurology and psychiatry.

[3]  O. Oscasson.  Functional organization of olivary projection to the cerebellar anterior lobe , 1980 .

[4]  J. Murphy,et al.  Differences between cerebellar mossy and climbing fibre responses to natural stimulation of forelimb muscle proprioceptors. , 1973, Brain research.

[5]  D. Armstrong,et al.  An investigation of the cerebellar corticonuclear projections in the rat using an autoradiographic tracing method. II. Projections from the hemisphere , 1978, Brain Research.

[6]  R. Eager,et al.  Efferent cortico‐nuclear pathways in the cerebellum of the cat , 1963 .

[7]  Eager Rp.  Patterns and mode of termination of cerebellar cortico-nuclear pathways in the monkey (Macaca mulatta). , 1966 .

[8]  F. Freemon,et al.  Functional localization in the cerebellum of the bird and its bearing on the evolution of cerebellar function , 1964, The Journal of comparative neurology.

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

[10]  T. Ebner,et al.  The changes in Purkinje cell simple spike activity following spontaneous climbing fiber inputs , 1982, Brain Research.

[11]  Kenneth D. Laxer,et al.  Somatotopic organization of climbing fiber projections from low threshold cutaneous afferents to pars intermedia of cerebellar cortex in the cat , 1980, Brain Research.

[12]  J. W. Lighthall,et al.  An HRP and autoradiographic study of the projection from the cerebellar cortex to the nucleus interpositus anterior and nucleus interpositus posterior of the cat , 1979, The Journal of comparative neurology.

[13]  A. Brodal,et al.  Olivocerebellar projection: a review. , 1980, Advances in anatomy, embryology, and cell biology.

[14]  J. Courville,et al.  Cerebellar corticonuclear projection in the cat. The paramedian lobule. An experimental study with silver methods. , 1973, Brain research.

[15]  J. Murphy,et al.  Responses of cerebellar cortical neurons to dynamic proprioceptive inputs from forelimb muscles. , 1973, Journal of neurophysiology.

[16]  W. Chambers,et al.  Functional localization in the cerebellum. I. Organization in longitudinal cortico‐nuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal , 1955, The Journal of comparative neurology.

[17]  D. Haines,et al.  Cerebellar corticonuclear fibers: Evidence of zones in the primate anterior lobe , 1977, Neuroscience Letters.

[18]  T. Ebner,et al.  Increase in Purkinje cell gain associated with naturally activated climbing fiber input. , 1983, Journal of neurophysiology.

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

[20]  G. M. Shambes,et al.  Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. , 1978, Brain, behavior and evolution.

[21]  D. C. Goodman,et al.  Patterns of localization in the cerebellar cortico‐nuclear projections of the albino rat , 1963 .

[22]  D. E. Haines,et al.  Organization of Cerebellar Corticonuclear Fiber Systems , 1982 .

[23]  O. Pompeiano,et al.  Identification of cerebellar corticovestibular neurons retrogradely labeled with horseradish peroxidase , 1979, Neuroscience.

[24]  J. Bloedel,et al.  Action of climbing fibers in cerebellar cortex of the cat. , 1971, Journal of neurophysiology.

[25]  D. Armstrong,et al.  Firing patterns of Purkinje cells in the cat cerebellum for different maintained positions of the limbs. , 1973, Brain research.

[26]  J. Eccles,et al.  The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum , 1966, The Journal of physiology.

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

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

[29]  W. T. Thach.  Somatosensory receptive fields of single units in cat cerebellar cortex. , 1967, Journal of neurophysiology.

[30]  Ray S. Snider,et al.  A stereotaxic atlas of the cat brain , 1987 .

[31]  T. Ebner,et al.  Role of climbing fiber afferent input in determining responsiveness of Purkinje cells to mossy fiber inputs. , 1981, Journal of neurophysiology.

[32]  J. Bloedel,et al.  Disorders of the cerebellum , 1981 .

[33]  W. Roberts,et al.  Climbing fiber responses of cerebellar Purkinje cells to passive movement of the cat forepaw , 1976, Brain Research.

[34]  D. Haines,et al.  Cerebellar corticonuclear fibers of the dorsal culminate lobule (anterior lobe—lobule V) in a prosimian primate, Galago senegalensis , 1979, The Journal of comparative neurology.