Crossref journal-article
Society for Neuroscience
The Journal of Neuroscience (393)
Abstract

Potentiation of spinal nociceptive transmission by synaptic delivery of AMPA receptors, via an NMDA receptor- and Ca2+/calmodulin-dependent protein kinase II (CaMKII)-dependent pathway, has been proposed to underlie certain forms of hyperalgesia, the enhanced pain sensitivity that may accompany inflammation or tissue injury. However, the specific synaptic populations that may be subject to such plasticity have not been identified. Using neuronal tracing and postembedding immunogold labeling, we show that a model of acute inflammatory hyperalgesia is associated with an elevated density of GluR1-containing AMPA receptors, as well as an increased synaptic ratio of GluR1 to GluR2/3 subunits, at synapses established by C-fibers that lack the neuropeptide substance P. A more subtle increase in GluR1 immunolabeling was noted at synapses formed by substance P-containing nociceptors. No changes in either GluR1 or GluR2/3 contents were observed at synapses formed by low-threshold mechanosensitive primary afferent fibers. These results contrast with our previous observations in the same pain model of increased and decreased levels of activated CaMKII at synapses formed by peptidergic and nonpeptidergic nociceptive fibers, respectively, suggesting that the observed redistribution of AMPA receptor subunits does not depend on postsynaptic CaMKII activity. The present ultrastructural evidence of topographically specific, activity-dependent insertion of GluR1-containing AMPA receptors at a central synapse suggests that potentiation of nonpeptidergic C-fiber synapses by this mechanism contributes to inflammatory pain.

Bibliography

Larsson, M., & Broman, J. (2008). Translocation of GluR1-Containing AMPA Receptors to a Spinal Nociceptive Synapse during Acute Noxious Stimulation. The Journal of Neuroscience, 28(28), 7084–7090.

Authors 2
  1. Max Larsson (first)
  2. Jonas Broman (additional)
References 44 Referenced 78
  1. 10.1016/j.neuron.2005.08.015
  2. 10.1038/sj.npp.1301559
  3. 10.1038/nrn2055
  4. 10.1038/nn997
  5. 10.1523/JNEUROSCI.22-10-04196.2002 / J Neurosci / Calcium-calmodulin-dependent protein kinase II contributes to spinal cord central sensitization by Fang (2002)
  6. 10.1016/j.pain.2004.09.011
  7. 10.1046/j.1460-9568.1999.00503.x
  8. 10.1126/science.287.5461.2262
  9. 10.1038/35053509
  10. 10.1126/science.1080659
  11. 10.1126/science.1127233
  12. 10.1016/j.tins.2003.09.017
  13. 10.1038/35093019
  14. 10.1111/j.1460-9568.2005.04081.x
  15. 10.1523/JNEUROSCI.0352-06.2006
  16. 10.1002/1096-9861(20010205)430:2<147::AID-CNE1021>3.0.CO;2-5
  17. 10.1038/nrn753
  18. 10.1016/j.neuroscience.2004.05.041
  19. 10.1016/0304-3940(95)11553-0
  20. 10.1126/science.278.5336.275
  21. 10.1523/JNEUROSCI.16-14-04457.1996 / J Neurosci / Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti by Matsubara (1996)
  22. 10.1073/pnas.95.26.15775
  23. 10.1016/0306-4522(91)90175-N
  24. 10.1523/JNEUROSCI.19-05-01844.1999 / J Neurosci / Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy by Michael (1999)
  25. 10.1016/S0301-0082(98)00048-3
  26. 10.1523/JNEUROSCI.1237-04.2004
  27. 10.1126/science.286.5444.1558
  28. 10.1016/j.brainres.2005.02.004
  29. 10.1038/4532
  30. 10.1186/1744-8069-4-5
  31. 10.1523/JNEUROSCI.16-10-03363.1996 / J Neurosci / AMPA receptor subunits underlying terminals of fine-caliber primary afferent fibers by Popratiloff (1996)
  32. 10.1523/JNEUROSCI.13-12-05228.1993 / J Neurosci / Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord by Randić (1993)
  33. Ribeiro-da-Silva A (2004) in The rat nervous system, Substantia gelatinosa of the spinal cord, ed Paxinos G (Elsevier, San Diego), Ed 3. (10.1016/B978-012547638-6/50007-9)
  34. 10.1016/S0304-3959(00)00424-3
  35. 10.1002/cne.903440307
  36. 10.1038/10172
  37. 10.1523/JNEUROSCI.22-10-04103.2002 / J Neurosci / Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance P-containing afferents and respond to noxious stimulation by Todd (2002)
  38. 10.1016/S0896-6273(00)80564-4
  39. 10.1016/S0306-4522(03)00125-8
  40. Willis WD Coggeshall RE (2004) Sensory mechanisms of the spinal cord (Kluwer Academic/Plenum, New York), Ed 3. (10.1007/978-1-4615-0037-7)
  41. 10.1152/jn.00735.2003
  42. 10.1016/j.neuroscience.2004.07.029
  43. 10.1016/0306-4522(93)90069-R
  44. 10.1038/80614
Dates
Type When
Created 17 years, 1 month ago (July 9, 2008, 12:23 p.m.)
Deposited 2 years, 4 months ago (April 13, 2023, 2:45 p.m.)
Indexed 3 months, 2 weeks ago (May 20, 2025, 8:11 a.m.)
Issued 17 years, 1 month ago (July 9, 2008)
Published 17 years, 1 month ago (July 9, 2008)
Published Online 17 years, 1 month ago (July 9, 2008)
Published Print 17 years, 1 month ago (July 9, 2008)
Funders 0

None

@article{Larsson_2008, title={Translocation of GluR1-Containing AMPA Receptors to a Spinal Nociceptive Synapse during Acute Noxious Stimulation}, volume={28}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.5749-07.2008}, DOI={10.1523/jneurosci.5749-07.2008}, number={28}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Larsson, Max and Broman, Jonas}, year={2008}, month=jul, pages={7084–7090} }