Home LiteratureArticle Details
PMID: 8308729 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Uniform olivocerebellar conduction time underlies Purkinje cell complex spike synchronicity in the rat cerebellum.

The Journal of physiology ·Vol. 470 ·1993-10-00 ·Pages 243-71

Sugihara I, Lang EJ, Llinás R

Abstract

1. The issue of isochronicity of olivocerebellar fibre conduction time as a basis for synchronizing complex spike activity in cerebellar Purkinje cells has been addressed by latency measurement, multiple-electrode recording and Phaseolus vulgaris leucoagglutinin (PHA-L) tracing of climbing fibres in the adult rat. 2. The conduction time of the olivocerebellar fibres was measured by recording Purkinje cell complex spike (CS) responses from various areas of the cerebellum. The CSs were evoked by stimulating the olivocerebellar fibres near the inferior olive. In spite of a difference in length, as determined directly by light microscopy, the conduction times of different climbing fibres were quite uniform, 3.98 +/- 0.36 ms (mean +/- S.D., n = 660). 3. Multiple-electrode recording of spontaneous Purkinje cell CS activity was employed to study the spatial extent of CS synchronicity in the cerebellar cortex. Recordings of CS were obtained from Purkinje cells located on the surface and along the walls of lobule crus 2a. The rostrocaudal band-like distribution of simultaneous (within 1 ms) CS activity in Purkinje cells extended down the sides of the cerebellar folia to the deepest areas recorded (1.6-2.6 mm deep). As shown in previous experiments, the distribution of simultaneous CS activity did not extend significantly (500 microns) in the mediolateral axis of the cerebellar cortex. 4. In two animals a detailed determination of the length of the olivocerebellar fibre bundles was performed by staining the fibres with PHA-L injected into the contralateral inferior olive. This measurement included fibre bundles terminating in twenty-six different areas, ranging from the tops of the various folia to the bottoms of the fissures in both the hemisphere and the vermis. There was a 47.5% difference between the length of the longest measured fibre bundle (15.8 mm, terminating in lobule 6b, zone A) and the length of the shortest measured fibre bundle (8.3 mm, terminating in the cortex at the base of the primary fissure, zone D), after correction for tissue shrinkage. To attain an isochronous conduction time the conduction velocities for these two fibre bundles were calculated to be 4.22 m/s and 2.37 m/s, respectively. 5. By interpolating between measured points a simple formula was derived to estimate the average length of olivocerebellar fibres terminating in any given area of the cerebellar cortex, excluding the paraflocculus, the flocculus and the most lateral regions of the hemisphere. 6. We investigated the most likely mechanisms by which conduction velocity variations with length could result in global isochronicity.(ABSTRACT TRUNCATED AT 400 WORDS)

MeSH Terms
Animals Axons/physiology Cerebellum/anatomy & histology,cytology,physiology Electric Stimulation Electrophysiology Microelectrodes Nerve Fibers/physiology Neural Conduction/physiology Neural Pathways/cytology,physiology Olivary Nucleus/anatomy & histology,cytology,physiology Purkinje Cells/physiology Rats Rats, Sprague-Dawley Reflex/physiology Stereotaxic Techniques
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Sugihara I
Department of Physiology and Biophysics, New York University Medical Center, NY 10016.
Lang E J
Llinás R
References (37)
37 references, click to expand
  1. Unitary multiple-spiked responses in cat inferior olive nucleus.
    J Neurophysiol. 1970 Mar;33(2):199-209 PMID: 4313283
  2. Responses in the inferior olive to stimulation of the cerebellar and cerebral cortices in the cat.
    J Physiol. 1966 Dec;187(3):553-74 PMID: 16783911
  3. The inferior olivary connections to the cerebellum in the rat studied by retrograde axonal transport of horseradish peroxidase.
    Brain Res Bull. 1980 May-Jun;5(3):267-75 PMID: 7397571
  4. Inhibitory control of intracerebellar nuclei by the purkinje cell axons.
    Exp Brain Res. 1970;10(1):64-80 PMID: 5411975
  5. Conduction velocity variations minimize conduction time differences among retinal ganglion cell axons.
    Science. 1987 Oct 16;238(4825):358-60 PMID: 3659918
  6. Climbing fibre induced depression of both mossy fibre responsiveness and glutamate sensitivity of cerebellar Purkinje cells.
    J Physiol. 1982 Mar;324:113-34 PMID: 7097592
  7. Functional significance of connections of the inferior olive.
    Physiol Rev. 1974 Apr;54(2):358-417 PMID: 4362162
  8. A circuit for detection of interaural time differences in the brain stem of the barn owl.
    J Neurosci. 1990 Oct;10(10):3227-46 PMID: 2213141
  9. The Functional Organization of the Olivo-Cerebellar System as Examined by Multiple Purkinje Cell Recordings.
    Eur J Neurosci. 1989 Jan;1(6):587-602 PMID: 12106117
  10. Ultrastructural study of the GABAergic, cerebellar, and mesodiencephalic innervation of the cat medial accessory olive: anterograde tracing combined with immunocytochemistry.
    J Comp Neurol. 1989 Jun 1;284(1):12-35 PMID: 2474000
  11. Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro.
    J Physiol. 1981 Jun;315:569-84 PMID: 7310722
  12. On the inferior olive of the albino rat.
    J Comp Neurol. 1970 Nov;140(3):255-60 PMID: 5476885
  13. Conduction velocity groups in the cat's optic nerve classified according to their retinal origin.
    Exp Brain Res. 1971 Nov 30;13(5):489-97 PMID: 5137298
  14. Cerebellar nucleo-olivary projections in the rat: an anterograde tracing study with Phaseolus vulgaris-leucoagglutinin (PHA-L).
    J Comp Neurol. 1990 Aug 15;298(3):315-33 PMID: 2212106
  15. Localization of glutamic-acid-decarboxylase-immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctions.
    J Comp Neurol. 1986 Oct 1;252(1):32-50 PMID: 3025270
  16. Branching of inferior olivary axons to terminate in different folia, lobules or lobes of the cerebellum.
    Brain Res. 1973 May 17;54:365-71 PMID: 4709152
  17. Reinnervation of cerebellar Purkinje cells by climbing fibres surviving a subtotal lesion of the inferior olive in the adult rat. I. Development of new collateral branches and terminal plexuses.
    J Comp Neurol. 1991 Jun 22;308(4):513-35 PMID: 1865015
  18. The spatial organisation of climbing fibre branching in the cat cerebellum.
    Exp Brain Res. 1973 Aug 31;18(1):40-58 PMID: 4746751
  19. Comparative physiology: electric organs.
    Annu Rev Physiol. 1970;32:471-528 PMID: 4906125
  20. Topographical localization in the olivocerebellar projection in the rat: an autoradiographic study.
    Brain Res. 1983 Sep 26;275(2):235-49 PMID: 6194853
  21. Anterograde tracing of the rat olivocerebellar system with Phaseolus vulgaris leucoagglutinin (PHA-L). Demonstration of climbing fiber collateral innervation of the cerebellar nuclei.
    J Comp Neurol. 1989 Oct 1;288(1):1-18 PMID: 2794133
  22. The parasagittal zonation within the olivocerebellar projection. I. Climbing fiber distribution in the vermis of cat cerebellum.
    J Comp Neurol. 1977 Aug 1;174(3):417-88 PMID: 903414
  23. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances.
    J Physiol. 1981 Jun;315:549-67 PMID: 6273544
  24. Eighteenth Bowditch lecture. Motor aspects of cerebellar control.
    Physiologist. 1974 Feb;17(1):19-46 PMID: 4361321
  25. Relations among climbing fiber responses of nearby Purkinje Cells.
    J Neurophysiol. 1972 Mar;35(2):155-69 PMID: 4337637
  26. Structural study of inferior olivary nucleus of the cat: morphological correlates of electrotonic coupling.
    J Neurophysiol. 1974 May;37(3):541-59 PMID: 4827021
  27. The climbing fibers of the cerebellar cortex, their origin and pathways in cat.
    Exp Brain Res. 1976 Nov 23;26(4):407-22 PMID: 63384
  28. Interaction experiments on the responses evoked in Purkinje cells by climbing fibres.
    J Physiol. 1966 Jan;182(2):297-315 PMID: 5942031
  29. Determinants of conduction velocity in myelinated nerve fibers.
    Muscle Nerve. 1980 Mar-Apr;3(2):141-50 PMID: 6245357
  30. Axonal branching in the climbing fiber pathway to the cerebellum.
    Brain Res. 1969 Sep;15(1):262-7 PMID: 5807773
  31. Relative conduction velocities of small myelinated and non-myelinated fibres in the central nervous system.
    Nat New Biol. 1972 Aug 16;238(85):217-9 PMID: 4506206
  32. Oscillatory properties of guinea-pig inferior olivary neurones and their pharmacological modulation: an in vitro study.
    J Physiol. 1986 Jul;376:163-82 PMID: 3795074
  33. Multiple Purkinje Cell Recording in Rodent Cerebellar Cortex.
    Eur J Neurosci. 1989 Jan;1(6):572-586 PMID: 12106116
  34. The excitatory synaptic action of climbing fibres on the Purkinje cells of the cerebellum.
    J Physiol. 1966 Jan;182(2):268-96 PMID: 5944665
  35. An approach to the quantitative analysis of electrophysiological data from single neurons.
    Biophys J. 1960 Sep;1:15-28 PMID: 13704760
  36. Anatomical demonstration of branching olivocerebellar fibres by means of a double retrograde labelling technique.
    Neuroscience. 1980;5(12):2193-202 PMID: 7465051
  37. Electrotonic coupling between neurons in cat inferior olive.
    J Neurophysiol. 1974 May;37(3):560-71 PMID: 4827022
Article Info
Journal
The Journal of physiology
Abbr.
J Physiol
ISSN
0022-3751
Published
1993-10-00
Pages
243-71
Language
English
Region
England
NLM ID
0266262
PMCID
PMC1143916
Subset
IM
Grants
NIGMS NIH HHS · NIGMH 5T32GMD07308 · United States
NINDS NIH HHS · NS13743 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]