Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Oct;87(20):8145–8149. doi: 10.1073/pnas.87.20.8145

When is an inhibitory synapse effective?

N Qian 1, T J Sejnowski 1
PMCID: PMC54909  PMID: 2236028

Abstract

Interactions between excitatory and inhibitory synaptic inputs on dendrites determine the level of activity in neurons. Models based on the cable equation predict that silent shunting inhibition can strongly veto the effect of an excitatory input. The cable model assumes that ionic concentrations do not change during the electrical activity, which may not be a valid assumption, especially for small structures such as dendritic spines. We present here an analysis and computer simulations to show that for large Cl- conductance changes, the more general Nernst-Planck electrodiffusion model predicts that shunting inhibition on spines should be much less effective than that predicted by the cable model. This is a consequence of the large changes in the intracellular ionic concentration of Cl- that can occur in small structures, which would alter the reversal potential and reduce the driving force for Cl-. Shunting inhibition should therefore not be effective on spines, but it could be significantly more effective on the dendritic shaft at the base of the spine. In contrast to shunting inhibition, hyperpolarizing synaptic inhibition mediated by K+ currents can be very effective in reducing the excitatory synaptic potentials on the same spine if the excitatory conductance change is less than 10 nS. We predict that if the inhibitory synapses found on cortical spines are to be effective, then they should be mediated by K+ through GABAB receptors.

Full text

PDF
8145

Selected References

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

  1. Beaulieu C., Colonnier M. A laminar analysis of the number of round-asymmetrical and flat-symmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. J Comp Neurol. 1985 Jan 8;231(2):180–189. doi: 10.1002/cne.902310206. [DOI] [PubMed] [Google Scholar]
  2. De Weer P., Rakowski R. F. Current generated by backward-running electrogenic Na pump in squid giant axons. 1984 May 31-Jun 6Nature. 309(5967):450–452. doi: 10.1038/309450a0. [DOI] [PubMed] [Google Scholar]
  3. Griffith W. H., Brown T. H., Johnston D. Voltage-clamp analysis of synaptic inhibition during long-term potentiation in hippocampus. J Neurophysiol. 1986 Apr;55(4):767–775. doi: 10.1152/jn.1986.55.4.767. [DOI] [PubMed] [Google Scholar]
  4. Harris K. M., Stevens J. K. Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics. J Neurosci. 1989 Aug;9(8):2982–2997. doi: 10.1523/JNEUROSCI.09-08-02982.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Higashima M., Sawada S., Yamamoto C. A revised method for generation of unitary postsynaptic potentials for quantal analysis in the hippocampus. Neurosci Lett. 1986 Jul 24;68(2):221–226. doi: 10.1016/0304-3940(86)90146-1. [DOI] [PubMed] [Google Scholar]
  6. Huguenard J. R., Alger B. E. Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons. J Neurophysiol. 1986 Jul;56(1):1–18. doi: 10.1152/jn.1986.56.1.1. [DOI] [PubMed] [Google Scholar]
  7. Janigro D., Schwartzkroin P. A. Effects of GABA on CA3 pyramidal cell dendrites in rabbit hippocampal slices. Brain Res. 1988 Jun 21;453(1-2):265–274. doi: 10.1016/0006-8993(88)90166-7. [DOI] [PubMed] [Google Scholar]
  8. Koch C., Poggio T. A theoretical analysis of electrical properties of spines. Proc R Soc Lond B Biol Sci. 1983 Jul 22;218(1213):455–477. doi: 10.1098/rspb.1983.0051. [DOI] [PubMed] [Google Scholar]
  9. Koch C., Poggio T., Torre V. Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci U S A. 1983 May;80(9):2799–2802. doi: 10.1073/pnas.80.9.2799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Koch C., Poggio T., Torre V. Retinal ganglion cells: a functional interpretation of dendritic morphology. Philos Trans R Soc Lond B Biol Sci. 1982 Jul 27;298(1090):227–263. doi: 10.1098/rstb.1982.0084. [DOI] [PubMed] [Google Scholar]
  11. Miles R., Wong R. K. Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J Physiol. 1984 Nov;356:97–113. doi: 10.1113/jphysiol.1984.sp015455. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES