Home LiteratureArticle Details
PMID: 14573542 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Receptive field plasticity profoundly alters the cutaneous parallel fiber synaptic input to cerebellar interneurons in vivo.

Jörntell H, Ekerot CF

Abstract

The cutaneous parallel fiber (PF) receptive fields of cerebellar stellate and basket cells in the cerebellar C3 zone in vivo are normally very small but can be dramatically enlarged by climbing fiber (CF)-dependent plasticity. To analyze the effects of this receptive field plasticity, we present for the first time whole-cell patch-clamp recordings from these interneurons during natural and electrical activation of cutaneously driven synaptic input. In "naive" interneurons, peripheral input nearly exclusively activated a few (two to eight) large PF EPSPs from a specific small skin area that overlapped the receptive field of the local CF input. After conjunctive PF and CF stimulation, numerous small and large EPSPs and ramp-like depolarizations could be activated from the entire forelimb skin. These findings therefore confirm previous suggestions that conjunctive PF and CF activation leads to a long-lasting potentiation of PF synaptic input to interneurons. The CF response, which is crucial for the induction of the PF synaptic potentiation, was strong but variable and very different from the conventional EPSPs evoked by PFs.

MeSH Terms
Afferent Pathways/physiology Animals Cats Cerebellum/cytology,physiology Decerebrate State Electric Stimulation Excitatory Postsynaptic Potentials/physiology Forelimb/innervation,physiology Interneurons/physiology Long-Term Potentiation/physiology Nerve Fibers/physiology Neural Inhibition/physiology Neuronal Plasticity/physiology Patch-Clamp Techniques Physical Stimulation Skin/innervation Synapses/physiology
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Jörntell Henrik
Department of Physiological Sciences, Section for Neurophysiology, SE-221 84 Lund, Sweden. henrik.jorntell@mphy.lu.se
Ekerot Carl-Fredrik
References (30)
30 references, click to expand
  1. Electrotonic coupling interacts with intrinsic properties to generate synchronized activity in cerebellar networks of inhibitory interneurons.
    J Neurosci. 1999 May 1;19(9):3298-306 PMID: 10212289
  2. Contributions of residual calcium to fast synaptic transmission.
    J Neurosci. 1999 Aug 1;19(15):6257-66 PMID: 10414955
  3. Morphology of single olivocerebellar axons labeled with biotinylated dextran amine in the rat.
    J Comp Neurol. 1999 Nov 15;414(2):131-48 PMID: 10516588
  4. A network of fast-spiking cells in the neocortex connected by electrical synapses.
    Nature. 1999 Nov 4;402(6757):72-5 PMID: 10573418
  5. Two networks of electrically coupled inhibitory neurons in neocortex.
    Nature. 1999 Nov 4;402(6757):75-9 PMID: 10573419
  6. A network of electrically coupled interneurons drives synchronized inhibition in neocortex.
    Nat Neurosci. 2000 Sep;3(9):904-10 PMID: 10966621
  7. Parallel fibre receptive fields of Purkinje cells and interneurons are climbing fibre-specific.
    Eur J Neurosci. 2001 Apr;13(7):1303-10 PMID: 11298790
  8. Spike transmission and synchrony detection in networks of GABAergic interneurons.
    Science. 2001 Jun 22;292(5525):2295-9 PMID: 11423653
  9. Cerebellar long-term depression: characterization, signal transduction, and functional roles.
    Physiol Rev. 2001 Jul;81(3):1143-95 PMID: 11427694
  10. Inhibition of interneuron firing extends the spread of endocannabinoid signaling in the cerebellum.
    Neuron. 2002 May 30;34(5):787-96 PMID: 12062024
  11. Reciprocal bidirectional plasticity of parallel fiber receptive fields in cerebellar Purkinje cells and their afferent interneurons.
    Neuron. 2002 May 30;34(5):797-806 PMID: 12062025
  12. Quantal events shape cerebellar interneuron firing.
    Nat Neurosci. 2002 Dec;5(12):1309-18 PMID: 12411959
  13. Properties of unitary granule cell-->Purkinje cell synapses in adult rat cerebellar slices.
    J Neurosci. 2002 Nov 15;22(22):9668-78 PMID: 12427822
  14. Coexistence of excitatory and inhibitory GABA synapses in the cerebellar interneuron network.
    J Neurosci. 2003 Mar 15;23(6):2019-31 PMID: 12657660
  15. Parallel fiber receptive fields: a key to understanding cerebellar operation and learning.
    Cerebellum. 2003;2(2):101-9 PMID: 12880177
  16. Purkinje cell activity during motor learning.
    Brain Res. 1977 Jun 10;128(2):309-28 PMID: 194656
  17. Complex spikes in Purkinje cells in the lateral vermis (b zone) of the cat cerebellum during locomotion.
    J Physiol. 1987 Apr;385:107-34 PMID: 3656160
  18. The length of parallel fibers in the cat cerebellar cortex. An experimental light and electron microscopic study.
    Exp Brain Res. 1976 Aug 27;26(1):39-58 PMID: 61126
  19. Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches.
    Pflugers Arch. 1981 Aug;391(2):85-100 PMID: 6270629
  20. Anatomy of cerebellar Purkinje cells in the rat determined by a specific immunohistochemical marker.
    Neuroscience. 1984 Apr;11(4):761-817 PMID: 6330609
  21. Prolonged depolarization elicited in Purkinje cell dendrites by climbing fibre impulses in the cat.
    J Physiol. 1981 Sep;318:207-21 PMID: 7320889
  22. Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices.
    J Physiol. 1980 Aug;305:197-213 PMID: 7441553
  23. IPSPs strongly inhibit climbing fiber-activated [Ca2+]i increases in the dendrites of cerebellar Purkinje neurons.
    J Neurosci. 1995 Apr;15(4):2777-87 PMID: 7722628
  24. Memory systems in the brain and localization of a memory.
    Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13438-44 PMID: 8942954
  25. Functional relation between corticonuclear input and movements evoked on microstimulation in cerebellar nucleus interpositus anterior in the cat.
    Exp Brain Res. 1995;106(3):365-76 PMID: 8983981
  26. Tonic synaptic inhibition modulates neuronal output pattern and spatiotemporal synaptic integration.
    Neuron. 1997 Sep;19(3):665-78 PMID: 9331356
  27. Impact of spontaneous synaptic activity on the resting properties of cat neocortical pyramidal neurons In vivo.
    J Neurophysiol. 1998 Mar;79(3):1450-60 PMID: 9497424
  28. Cerebellar complex spikes encode both destinations and errors in arm movements.
    Nature. 1998 Apr 2;392(6675):494-7 PMID: 9548253
  29. Quantitative Golgi study of the rat cerebellar molecular layer interneurons using principal component analysis.
    J Comp Neurol. 1998 Apr 13;393(3):353-73 PMID: 9548555
  30. Cutaneous receptive fields and topography of mossy fibres and climbing fibres projecting to cat cerebellar C3 zone.
    J Physiol. 1998 Oct 1;512 ( Pt 1):277-93 PMID: 9729638
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
2003-10-22
Pages
9620-31
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6740478
Subset
IM
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: product@genelibs.com