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. 1989 Feb;409:157–170. doi: 10.1113/jphysiol.1989.sp017490

Synaptic control of excitability in turtle cerebellar Purkinje cells.

J Hounsgaard 1, J Midtgaard 1
PMCID: PMC1190437  PMID: 2585289

Abstract

1. In turtle Purkinje cells in vitro successive climbing fibre responses (CFRs) gradually induced a hyperpolarization that persisted with maintained stimulation and decayed over minutes after climbing fibre stimulation was terminated. 2. The rate of development and the amplitude of this long-lasting hyperpolarization (LHP) increased with the frequency of CFRs. 3. The LHP was also induced by Ca2+ spikes evoked by current injection but not by Na+ spikes. The LHP was blocked by Co2+ but not by tetrodotoxin and could not be explained solely by an increased K+ conductance. 4. Depolarizing current during a train of CFRs enhanced the regenerative component of CFRs and promoted the LHP. Hyperpolarizing current during the stimulus train reduced the regenerative component of CFRs and attenuated the resulting LHP. 5. In the range of membrane potentials attained at different levels of climbing fibre activity the regenerative component of CFRs varied from being dominant at very low stimulus frequency (0.1 s-1) to being inconspicuous at high stimulus frequency (10 s-1). 6. It is concluded that successive CFRs induce a Ca2+-dependent, long-lasting hyperpolarization. The magnitude of the hyperpolarization is regulated by the rate of CFRs and by the voltage- and frequency-dependent configuration of each individual CFR. 7. The active, non-synaptic properties of turtle Purkinje cells make the Ca2+ influx during climbing fibre responses prone to regulation by on-going synaptic activity and by the after-effects of synaptic activity on a time scale of minutes. We suggest that this arrangement may enhance the capacity and complexity of spatial and temporal synaptic integration in Purkinje cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersson G., Hesslow G. Activity of Purkinje cells and interpositus neurones during and after periods of high frequency climbing fibre activation in the cat. Exp Brain Res. 1987;67(3):533–542. doi: 10.1007/BF00247286. [DOI] [PubMed] [Google Scholar]
  2. Batini C., Billard J. M. Release of cerebellar inhibition by climbing fiber deafferentation. Exp Brain Res. 1985;57(2):370–380. doi: 10.1007/BF00236543. [DOI] [PubMed] [Google Scholar]
  3. Chan C. Y., Hounsgaard J., Midtgaard J. Excitatory synaptic responses in turtle cerebellar Purkinje cells. J Physiol. 1989 Feb;409:143–156. doi: 10.1113/jphysiol.1989.sp017489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Chan C. Y., Hounsgaard J., Nicholson C. Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. J Physiol. 1988 Aug;402:751–771. doi: 10.1113/jphysiol.1988.sp017232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Colin F., Manil J., Desclin J. C. The olivocerebellar system. I. Delayed and slow inhibitory effects: an overlooked salient feature of cerebellar climbing fibers. Brain Res. 1980 Apr 7;187(1):3–27. doi: 10.1016/0006-8993(80)90491-6. [DOI] [PubMed] [Google Scholar]
  6. Crepel F., Dhanjal S. S., Garthwaite J. Morphological and electrophysiological characteristics of rat cerebellar slices maintained in vitro. J Physiol. 1981 Jul;316:127–138. doi: 10.1113/jphysiol.1981.sp013777. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ferrendelli J. A., Rubin E. H., Kinscherf D. A. Influence of divalent cations on regulation of cyclic GMP and cyclic AMP levels in brain tissue. J Neurochem. 1976 Apr;26(4):741–748. doi: 10.1111/j.1471-4159.1976.tb04447.x. [DOI] [PubMed] [Google Scholar]
  8. GRANIT R., PHILLIPS C. G. Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J Physiol. 1956 Sep 27;133(3):520–547. doi: 10.1113/jphysiol.1956.sp005606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ghelarducci B., Ito M., Yagi N. Impulse discharges from flocculus Purkinje cells of alert rabbits during visual stimulation combined with horizontal head rotation. Brain Res. 1975 Apr 4;87(1):66–72. doi: 10.1016/0006-8993(75)90780-5. [DOI] [PubMed] [Google Scholar]
  10. Gilbert P. F., Thach W. T. Purkinje cell activity during motor learning. Brain Res. 1977 Jun 10;128(2):309–328. doi: 10.1016/0006-8993(77)90997-0. [DOI] [PubMed] [Google Scholar]
  11. Guidotti A., Biggio G., Costa E. 3-Acetylpyridine: a tool to inhibit the tremor and the increase of cGMP content in cerebellar cortex elicited by harmaline. Brain Res. 1975 Oct 10;96(1):201–205. doi: 10.1016/0006-8993(75)90598-3. [DOI] [PubMed] [Google Scholar]
  12. Hounsgaard J., Hultborn H., Jespersen B., Kiehn O. Intrinsic membrane properties causing a bistable behaviour of alpha-motoneurones. Exp Brain Res. 1984;55(2):391–394. doi: 10.1007/BF00237290. [DOI] [PubMed] [Google Scholar]
  13. Hounsgaard J., Midtgaard J. Intrinsic determinants of firing pattern in Purkinje cells of the turtle cerebellum in vitro. J Physiol. 1988 Aug;402:731–749. doi: 10.1113/jphysiol.1988.sp017231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jahnsen H., Llinás R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J Physiol. 1984 Apr;349:205–226. doi: 10.1113/jphysiol.1984.sp015153. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. KANDEL E. R., SPENCER W. A. Electrophysiology of hippocampal neurons. II. After-potentials and repetitive firing. J Neurophysiol. 1961 May;24:243–259. doi: 10.1152/jn.1961.24.3.243. [DOI] [PubMed] [Google Scholar]
  16. Llinas R., Nicholson C. Electrophysiological properties of dendrites and somata in alligator Purkinje cells. J Neurophysiol. 1971 Jul;34(4):532–551. doi: 10.1152/jn.1971.34.4.532. [DOI] [PubMed] [Google Scholar]
  17. Llinás R., Hess R. Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. Proc Natl Acad Sci U S A. 1976 Jul;73(7):2520–2523. doi: 10.1073/pnas.73.7.2520. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. J Physiol. 1980 Aug;305:197–213. doi: 10.1113/jphysiol.1980.sp013358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Llinás R., Sugimori M. Electrophysiological properties of in vitro Purkinje cell somata in mammalian cerebellar slices. J Physiol. 1980 Aug;305:171–195. doi: 10.1113/jphysiol.1980.sp013357. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Masukawa L. M., Prince D. A. Synaptic control of excitability in isolated dendrites of hippocampal neurons. J Neurosci. 1984 Jan;4(1):217–227. doi: 10.1523/JNEUROSCI.04-01-00217.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Montarolo P. G., Palestini M., Strata P. The inhibitory effect of the olivocerebellar input on the cerebellar Purkinje cells in the rat. J Physiol. 1982 Nov;332:187–202. doi: 10.1113/jphysiol.1982.sp014409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Rawson J. A., Tilokskulchai K. Climbing fibre modification of cerebellar Purkinje cell responses to parallel fibre inputs. Brain Res. 1982 Apr 15;237(2):492–497. doi: 10.1016/0006-8993(82)90461-9. [DOI] [PubMed] [Google Scholar]
  23. Ross W. N., Werman R. Mapping calcium transients in the dendrites of Purkinje cells from the guinea-pig cerebellum in vitro. J Physiol. 1987 Aug;389:319–336. doi: 10.1113/jphysiol.1987.sp016659. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sakurai M. Synaptic modification of parallel fibre-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J Physiol. 1987 Dec;394:463–480. doi: 10.1113/jphysiol.1987.sp016881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Savio T., Tempia F. On the Purkinje cell activity increase induced by suppression of inferior olive activity. Exp Brain Res. 1985;57(3):456–463. doi: 10.1007/BF00237832. [DOI] [PubMed] [Google Scholar]

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