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. 1991;440:723–734. doi: 10.1113/jphysiol.1991.sp018732

Excitation by geniculocortical synapses is not 'vetoed' at the level of dendritic spines in cat visual cortex.

C Dehay 1, R J Douglas 1, K A Martin 1, C Nelson 1
PMCID: PMC1180176  PMID: 1804984

Abstract

1. We used anatomical methods to examine whether the geniculocortical afferent input to dendritic spines could be gated or 'vetoed' by an inhibitory input to the same spine. 2. Physiologically identified X- and Y-type afferents were injected intra-axonally with horseradish peroxidase (HRP), processed, and drawn under the light microscope. Selected regions of the terminal arbors were then serially sectioned for examination under the electron microscope. 3. Three-dimensional reconstructions of thirty-nine HRP-filled terminal boutons forming fifty asymmetric (type 1) synapses showed that thirty-one synapses were on the heads of dendritic spines. Only two of thirty-one spine heads received an additional symmetric (type 2) synapse, which is presumed to be inhibitory. 4. Examination of twenty-three boutons from two clutch cells (a GABA (gamma-aminobutyric acid)-ergic smooth cell) that form symmetric (type 2) synapses on spines indicated that their preferred location was opposite the asymmetric synapse on the head of the spine. Synaptic input to the necks of spines appears rare. 5. We conclude that most of the excitation provided by the geniculocortical afferent input to the heads of spines cannot be gated or vetoed by inhibition at the level of the spine.

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Selected References

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  1. Adams J. C. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem. 1981 Jun;29(6):775–775. doi: 10.1177/29.6.7252134. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Berman N. J., Douglas R. J., Martin K. A., Whitteridge D. Mechanisms of inhibition in cat visual cortex. J Physiol. 1991;440:697–722. doi: 10.1113/jphysiol.1991.sp018731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bullier J., Henry G. H. Ordinal position of neurons in cat striate cortex. J Neurophysiol. 1979 Sep;42(5):1251–1263. doi: 10.1152/jn.1979.42.5.1251. [DOI] [PubMed] [Google Scholar]
  5. Douglas R. J., Martin K. A., Whitteridge D. Selective responses of visual cortical cells do not depend on shunting inhibition. Nature. 1988 Apr 14;332(6165):642–644. doi: 10.1038/332642a0. [DOI] [PubMed] [Google Scholar]
  6. Ferster D., Lindström S. An intracellular analysis of geniculo-cortical connectivity in area 17 of the cat. J Physiol. 1983 Sep;342:181–215. doi: 10.1113/jphysiol.1983.sp014846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Freund T. F., Martin K. A., Somogyi P., Whitteridge D. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. J Comp Neurol. 1985 Dec 8;242(2):275–291. doi: 10.1002/cne.902420209. [DOI] [PubMed] [Google Scholar]
  8. Freund T. F., Martin K. A., Whitteridge D. Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y- type thalamic afferents. I. Arborization patterns and quantitative distribution of postsynaptic elements. J Comp Neurol. 1985 Dec 8;242(2):263–274. doi: 10.1002/cne.902420208. [DOI] [PubMed] [Google Scholar]
  9. GRAY E. G. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat. 1959 Oct;93:420–433. [PMC free article] [PubMed] [Google Scholar]
  10. Gabbott P. L., Martin K. A., Whitteridge D. Evidence for the connections between a clutch cell and a corticotectal neuron in area 17 of the cat visual cortex. Proc R Soc Lond B Biol Sci. 1988 May 23;233(1273):385–391. doi: 10.1098/rspb.1988.0028. [DOI] [PubMed] [Google Scholar]
  11. Garey L. J., Powell T. P. An experimental study of the termination of the lateral geniculo-cortical pathway in the cat and monkey. Proc R Soc Lond B Biol Sci. 1971 Oct 12;179(1054):41–63. doi: 10.1098/rspb.1971.0080. [DOI] [PubMed] [Google Scholar]
  12. Gilbert C. D., Wiesel T. N. Clustered intrinsic connections in cat visual cortex. J Neurosci. 1983 May;3(5):1116–1133. doi: 10.1523/JNEUROSCI.03-05-01116.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hanker J. S., Yates P. E., Metz C. B., Rustioni A. A new specific, sensitive and non-carcinogenic reagent for the demonstration of horseradish peroxidase. Histochem J. 1977 Nov;9(6):789–792. doi: 10.1007/BF01003075. [DOI] [PubMed] [Google Scholar]
  14. Hornung J. P., Garey L. J. The thalamic projection to cat visual cortex: ultrastructure of neurons identified by Golgi impregnation or retrograde horseradish peroxidase transport. Neuroscience. 1981;6(6):1053–1068. doi: 10.1016/0306-4522(81)90070-1. [DOI] [PubMed] [Google Scholar]
  15. Jones E. G., Powell T. P. Morphological variations in the dendritic spines of the neocortex. J Cell Sci. 1969 Sep;5(2):509–529. doi: 10.1242/jcs.5.2.509. [DOI] [PubMed] [Google Scholar]
  16. 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]
  17. LeVay S., Gilbert C. D. Laminar patterns of geniculocortical projection in the cat. Brain Res. 1976 Aug 20;113(1):1–19. doi: 10.1016/0006-8993(76)90002-0. [DOI] [PubMed] [Google Scholar]
  18. Martin K. A. The Wellcome Prize lecture. From single cells to simple circuits in the cerebral cortex. Q J Exp Physiol. 1988 Sep;73(5):637–702. doi: 10.1113/expphysiol.1988.sp003190. [DOI] [PubMed] [Google Scholar]
  19. Martin K. A., Whitteridge D. Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. J Physiol. 1984 Aug;353:463–504. doi: 10.1113/jphysiol.1984.sp015347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Perry V. H., Linden R. Evidence for dendritic competition in the developing retina. Nature. 1982 Jun 24;297(5868):683–685. doi: 10.1038/297683a0. [DOI] [PubMed] [Google Scholar]
  21. Peters A., Kaiserman-Abramof I. R. The small pyramidal neuron of the rat cerebral cortex. The perikaryon, dendrites and spines. Am J Anat. 1970 Apr;127(4):321–355. doi: 10.1002/aja.1001270402. [DOI] [PubMed] [Google Scholar]
  22. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sloper J. J., Powell T. P. An experimental electron microscopic study of afferent connections to the primate motor and somatic sensory cortices. Philos Trans R Soc Lond B Biol Sci. 1979 Mar 23;285(1006):199–226. doi: 10.1098/rstb.1979.0005. [DOI] [PubMed] [Google Scholar]
  24. Somogyi P., Soltész I. Immunogold demonstration of GABA in synaptic terminals of intracellularly recorded, horseradish peroxidase-filled basket cells and clutch cells in the cat's visual cortex. Neuroscience. 1986 Dec;19(4):1051–1065. doi: 10.1016/0306-4522(86)90122-3. [DOI] [PubMed] [Google Scholar]

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