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Journal of Neuroscience, Vol 13, 5228-5241, Copyright © 1993 by Society for Neuroscience
Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord
M Randic, MC Jiang and R Cerne
Department of Veterinary Physiology and Pharmacology, Iowa State University, Ames 50011.
Synaptic transmission between dorsal root afferents and neurons in the
superficial laminae of the spinal dorsal horn (laminae I-III) was examined
by intracellular recording in a transverse slice preparation of rat spinal
cord. Brief high-frequency electrical stimulation (300 pulses at 100 Hz) of
primary afferent fibers produced a long-term potentiation (LTP) or a
long-term depression (LTD) of fast (monosynaptic and polysynaptic) EPSPs in
a high proportion of dorsal horn neurons. Both the AMPA and the NMDA
receptor-mediated components of synaptic transmission at the primary
afferent synapses with neurons in the dorsal horn can exhibit LTP and LTD
of the synaptic responses. In normal and neonatally capsaicin-treated rats,
the induction of LTP requires the activation of NMDA receptor-gated
conductances. The induction of LTP or LTD, however, was not abolished in
the presence of bicuculline, a GABAA receptor antagonist. The results
demonstrate that distinct and long-lasting modulation in synaptic
efficiency can be induced at primary afferent synapses with neurons in the
superficial laminae of spinal dorsal horn by high-frequency stimulation of
dorsal root afferents and that these changes may be physiologically
relevant for transmission and integration of sensory information, including
pain.
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|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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March 1, 2003;
23(5):
1847 - 1858.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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May 15, 2002;
22(10):
4196 - 4204.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
S. Chiechio, A. Caricasole, E. Barletta, M. Storto, M. V. Catania, A. Copani, M. Vertechy, R. Nicolai, M. Calvani, D. Melchiorri, et al.
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May 1, 2002;
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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June 15, 2001;
21(12):
4469 - 4477.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
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J Neurophysiol,
May 1, 2001;
85(5):
1864 - 1872.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Barbieri and A. Nistri
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April 1, 2001;
85(4):
1502 - 1511.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
W. D. Willis Jr.
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Ann. N.Y. Acad. Sci.,
March 1, 2001;
933(1):
142 - 156.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
G. W. Terman, C. L. Eastman, and C. Chavkin
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J Neurophysiol,
February 1, 2001;
85(2):
485 - 494.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. J. Woolf and M. W. Salter
Neuronal Plasticity: Increasing the Gain in Pain
Science,
June 9, 2000;
288(5472):
1765 - 1768.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Ikeda, T. Asai, and K. Murase
Robust Changes of Afferent-Induced Excitation in the Rat Spinal Dorsal Horn After Conditioning High-Frequency Stimulation
J Neurophysiol,
April 1, 2000;
83(4):
2412 - 2420.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
I. Kohama, K. Ishikawa, and J. D. Kocsis
Synaptic Reorganization in the Substantia Gelatinosa After Peripheral Nerve Neuroma Formation: Aberrant Innervation of Lamina II Neurons by Abeta Afferents
J. Neurosci.,
February 15, 2000;
20(4):
1538 - 1549.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Levinsson, X.-L. Luo, H. Holmberg, and J. Schouenborg
Developmental Tuning in a Spinal Nociceptive System: Effects of Neonatal Spinalization
J. Neurosci.,
December 1, 1999;
19(23):
10397 - 10403.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Ikeda, T. Asai, M. Randic, and K. Murase
Robust Suppression of Afferent-Induced Excitation in the Rat Spinal Dorsal Horn After Conditioning Low-Frequency Stimulation
J Neurophysiol,
October 1, 1999;
82(4):
1957 - 1964.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X.-M. Yu and M. W. Salter
Src, a molecular switch governing gain control of synaptic transmission mediated by N-methyl-D-aspartate receptors
PNAS,
July 6, 1999;
96(14):
7697 - 7704.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Li, A. A. Calejesan, and M. Zhuo
ATP P2× Receptors and Sensory Synaptic Transmission Between Primary Afferent Fibers and Spinal Dorsal Horn Neurons in Rats
J Neurophysiol,
December 1, 1998;
80(6):
3356 - 3360.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. E. Schwartz and S. Alford
Modulation of Pre- and Postsynaptic Calcium Dynamics by Ionotropic Glutamate Receptors at a Plastic Synapse
J Neurophysiol,
April 1, 1998;
79(4):
2191 - 2203.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Gozariu, D. Bragard, J.-C. Willer, and D. Le Bars
Temporal Summation of C-Fiber Afferent Inputs: Competition Between Facilitatory and Inhibitory Effects on C-Fiber Reflex in the Rat
J Neurophysiol,
December 1, 1997;
78(6):
3165 - 3179.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. C. G. Marvizon, V. Martinez, E. F. Grady, N. W. Bunnett, and E. A. Mayer
Neurokinin 1 Receptor Internalization in Spinal Cord Slices Induced by Dorsal Root Stimulation Is Mediated by NMDA Receptors
J. Neurosci.,
November 1, 1997;
17(21):
8129 - 8136.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
X.-G. Liu and J. Sandkuhler
Characterization of Long-Term Potentiation of C-Fiber-Evoked Potentials in Spinal Dorsal Horn of Adult Rat: Essential Role of NK1 and NK2 Receptors
J Neurophysiol,
October 1, 1997;
78(4):
1973 - 1982.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. B. Malmberg, E. P. Brandon, R. L. Idzerda, H. Liu, G. S. McKnight, and A. I. Basbaum
Diminished Inflammation and Nociceptive Pain with Preservation of Neuropathic Pain in Mice with a Targeted Mutation of the Type I Regulatory Subunit of cAMP-Dependent Protein Kinase
J. Neurosci.,
October 1, 1997;
17(19):
7462 - 7470.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
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J. Sandkuhler, J. G. Chen, and G. Cheng
Low-Frequency Stimulation of Afferent Adelta -Fibers Induces Long-Term Depression at Primary Afferent Synapses with Substantia Gelatinosa Neurons in the Rat
J. Neurosci.,
August 15, 1997;
17(16):
6483 - 6491.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
Z. Zhou, J. Champagnat, and C.-S. Poon
Phasic and Long-Term Depression in Brainstem Nucleus Tractus Solitarius Neurons: Differing Roles of AMPA Receptor Desensitization
J. Neurosci.,
July 15, 1997;
17(14):
5349 - 5356.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R.-R. Ji and F. Rupp
Phosphorylation of Transcription Factor CREB in Rat Spinal Cord after Formalin-Induced Hyperalgesia: Relationship to c-fos Induction
J. Neurosci.,
March 1, 1997;
17(5):
1776 - 1785.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
K. S. Vikman, K. Kristensson, and R. H. Hill
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October 1, 2001;
21(19):
RC169 - RC169.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
