Crossref journal-article
Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences (341)
Abstract

Neocortical acetylcholine (ACH) release is known to enhance signal processing by increasing the amplitude and signal-to-noise ratio (SNR) of sensory responses. It is widely accepted that the larger sensory responses are caused by a persistent increase in the excitability of all cortical excitatory neurons. Here, contrary to this concept, we show that ACH persistently inhibits layer 4 (L4) spiny neurons, the main targets of thalamocortical inputs. Using whole-cell recordings in slices of rat primary somatosensory cortex, we demonstrate that this inhibition is specific to L4 and contrasts with the ACH-induced persistent excitation of pyramidal cells in L2/3 and L5. We find that this inhibition is induced by postsynaptic M4-muscarinic ACH receptors and is mediated by the opening of inwardly rectifying potassium (Kir) channels. Pair recordings of L4 spiny neurons show that ACH reduces synaptic release in the L4 recurrent microcircuit. We conclude that ACH has a differential layer-specific effect that results in a filtering of weak sensory inputs in the L4 recurrent excitatory microcircuit and a subsequent amplification of relevant inputs in L2/3 and L5 excitatory microcircuits. This layer-specific effect may contribute to improve cortical SNR.

Bibliography

Eggermann, E., & Feldmeyer, D. (2009). Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4. Proceedings of the National Academy of Sciences, 106(28), 11753–11758.

Authors 2
  1. Emmanuel Eggermann (first)
  2. Dirk Feldmeyer (additional)
References 46 Referenced 90
  1. 10.1016/j.tips.2005.09.009
  2. 10.1016/S0926-6410(00)00012-4
  3. 10.1016/0006-8993(87)90407-0
  4. 10.1152/jn.1987.58.4.765
  5. 10.1016/0006-8993(83)90015-X
  6. 10.1038/291554a0
  7. 10.1523/JNEUROSCI.15-02-01099.1995
  8. 10.1016/j.neuron.2006.08.005
  9. 10.1523/JNEUROSCI.4310-05.2006
  10. 10.1523/JNEUROSCI.2697-05.2005
  11. 10.1523/JNEUROSCI.19-05-01599.1999
  12. 10.1113/jphysiol.1986.sp016112
  13. 10.1146/annurev.pharmtox.47.120505.105214
  14. 10.1016/S0079-6123(03)45015-2
  15. K Krnjevic, Synaptic mechanisms modulated by acetylcholine in cerebral cortex. Prog Brain Res 145, 81–93 (2004). / Prog Brain Res / Synaptic mechanisms modulated by acetylcholine in cerebral cortex by Krnjevic K (2004)
  16. 10.1016/S0166-4328(00)00259-X
  17. 10.1016/S0896-6273(00)80380-3
  18. 10.1016/S0006-8993(00)02766-9
  19. 10.1016/S0306-4522(02)00663-2
  20. 10.1523/JNEUROSCI.20-14-05300.2000
  21. 10.1111/j.1469-7793.1999.00169.x
  22. 10.1016/S0959-4388(00)00239-7
  23. 10.1523/JNEUROSCI.10-08-02638.1990
  24. 10.1038/nn1690
  25. 10.1073/pnas.82.18.6344
  26. MP Caulfield, NJ Birdsall, International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50, 279–290 (1998). (10.1016/S0031-6997(24)01362-0) / Pharmacol Rev / International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors by Caulfield MP (1998)
  27. 10.1111/j.1749-6632.1999.tb11293.x
  28. 10.1111/j.1469-7793.2001.00383.x
  29. 10.1016/j.neuron.2007.08.025
  30. 10.1152/jn.00493.2006
  31. 10.1523/JNEUROSCI.19-14-05693.1999
  32. 10.1016/S0896-6273(00)80479-1
  33. 10.1038/319405a0
  34. 10.1016/S0306-4522(97)00167-X
  35. 10.1038/319402a0
  36. 10.1113/jphysiol.2003.044222
  37. 10.1113/jphysiol.2006.124321
  38. 10.1007/s00359-006-0117-6
  39. 10.1152/jn.00828.2006
  40. 10.1523/JNEUROSCI.11-10-03218.1991
  41. 10.1523/JNEUROSCI.08-12-04646.1988
  42. 10.1523/JNEUROSCI.21-08-02699.2001
  43. 10.1016/j.neuron.2005.09.022
  44. 10.1016/S0301-0082(98)00084-7
  45. 10.1126/science.1124593
  46. 10.1093/cercor/13.1.33
Dates
Type When
Created 16 years, 2 months ago (June 29, 2009, 9:42 p.m.)
Deposited 6 months, 3 weeks ago (Feb. 10, 2025, 9:01 a.m.)
Indexed 3 months, 2 weeks ago (May 14, 2025, 2:43 p.m.)
Issued 16 years, 1 month ago (July 14, 2009)
Published 16 years, 1 month ago (July 14, 2009)
Published Online 16 years, 1 month ago (July 14, 2009)
Published Print 16 years, 1 month ago (July 14, 2009)
Funders 0

None

@article{Eggermann_2009, title={Cholinergic filtering in the recurrent excitatory microcircuit of cortical layer 4}, volume={106}, ISSN={1091-6490}, url={http://dx.doi.org/10.1073/pnas.0810062106}, DOI={10.1073/pnas.0810062106}, number={28}, journal={Proceedings of the National Academy of Sciences}, publisher={Proceedings of the National Academy of Sciences}, author={Eggermann, Emmanuel and Feldmeyer, Dirk}, year={2009}, month=jul, pages={11753–11758} }