Skip to main content
PMC home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1996 Nov 1;496(Pt 3):597–606. doi: 10.1113/jphysiol.1996.sp021711

A linear model fails to predict orientation selectivity of cells in the cat visual cortex.

M Volgushev 1, T R Vidyasagar 1, X Pei 1
PMCID: PMC1160848  PMID: 8930828

Abstract

1. Postsynaptic potentials (PSPs) evoked by visual stimulation in simple cells in the cat visual cortex were recorded using in vivo whole-cell technique. Responses to small spots of light presented at different positions over the receptive field and responses to elongated bars of different orientations centred on the receptive field were recorded. 2. To test whether a linear model can account for orientation selectivity of cortical neurones, responses to elongated bars were compared with responses predicted by a linear model from the receptive field map obtained from flashing spots. 3. The linear model faithfully predicted the preferred orientation, but not the degree of orientation selectivity or the sharpness of orientation tuning. The ratio of optimal to non-optimal responses was always underestimated by the model. 4. Thus non-linear mechanisms, which can include suppression of non-optimal responses and/or amplification of optimal responses, are involved in the generation of orientation selectivity in the primary visual cortex.

Full text

PDF
597

Selected References

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

  1. Bonds A. B. Role of inhibition in the specification of orientation selectivity of cells in the cat striate cortex. Vis Neurosci. 1989;2(1):41–55. doi: 10.1017/s0952523800004314. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Chapman B., Zahs K. R., Stryker M. P. Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J Neurosci. 1991 May;11(5):1347–1358. doi: 10.1523/JNEUROSCI.11-05-01347.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DeAngelis G. C., Ohzawa I., Freeman R. D. Spatiotemporal organization of simple-cell receptive fields in the cat's striate cortex. II. Linearity of temporal and spatial summation. J Neurophysiol. 1993 Apr;69(4):1118–1135. doi: 10.1152/jn.1993.69.4.1118. [DOI] [PubMed] [Google Scholar]
  5. Dean A. F., Tolhurst D. J., Walker N. S. Non-linear temporal summation by simple cells in cat striate cortex demonstrated by failure of superposition. Exp Brain Res. 1982;45(3):456–458. doi: 10.1007/BF01208607. [DOI] [PubMed] [Google Scholar]
  6. Douglas R. J., Koch C., Mahowald M., Martin K. A., Suarez H. H. Recurrent excitation in neocortical circuits. Science. 1995 Aug 18;269(5226):981–985. doi: 10.1126/science.7638624. [DOI] [PubMed] [Google Scholar]
  7. Douglas R. J., Martin K. A. A functional microcircuit for cat visual cortex. J Physiol. 1991;440:735–769. doi: 10.1113/jphysiol.1991.sp018733. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ferster D. Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci. 1986 May;6(5):1284–1301. doi: 10.1523/JNEUROSCI.06-05-01284.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. HUBEL D. H., WIESEL T. N. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex. J Physiol. 1962 Jan;160:106–154. doi: 10.1113/jphysiol.1962.sp006837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Heggelund P., Moors J. Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells. Exp Brain Res. 1983;52(2):235–247. doi: 10.1007/BF00236632. [DOI] [PubMed] [Google Scholar]
  11. Henry G. H., Michalski A., Wimborne B. M., McCart R. J. The nature and origin of orientation specificity in neurons of the visual pathways. Prog Neurobiol. 1994 Jul-Aug;43(4-5):381–437. doi: 10.1016/0301-0082(94)90061-2. [DOI] [PubMed] [Google Scholar]
  12. Hirsch J. A. Synaptic integration in layer IV of the ferret striate cortex. J Physiol. 1995 Feb 15;483(Pt 1):183–199. doi: 10.1113/jphysiol.1995.sp020577. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Huguenard J. R., Hamill O. P., Prince D. A. Sodium channels in dendrites of rat cortical pyramidal neurons. Proc Natl Acad Sci U S A. 1989 Apr;86(7):2473–2477. doi: 10.1073/pnas.86.7.2473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jagadeesh B., Wheat H. S., Ferster D. Linearity of summation of synaptic potentials underlying direction selectivity in simple cells of the cat visual cortex. Science. 1993 Dec 17;262(5141):1901–1904. doi: 10.1126/science.8266083. [DOI] [PubMed] [Google Scholar]
  15. Morrone M. C., Burr D. C., Maffei L. Functional implications of cross-orientation inhibition of cortical visual cells. I. Neurophysiological evidence. Proc R Soc Lond B Biol Sci. 1982 Oct 22;216(1204):335–354. doi: 10.1098/rspb.1982.0078. [DOI] [PubMed] [Google Scholar]
  16. Movshon J. A., Thompson I. D., Tolhurst D. J. Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol. 1978 Oct;283:53–77. doi: 10.1113/jphysiol.1978.sp012488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Nelson S., Toth L., Sheth B., Sur M. Orientation selectivity of cortical neurons during intracellular blockade of inhibition. Science. 1994 Aug 5;265(5173):774–777. doi: 10.1126/science.8047882. [DOI] [PubMed] [Google Scholar]
  18. Pei X., Vidyasagar T. R., Volgushev M., Creutzfeldt O. D. Receptive field analysis and orientation selectivity of postsynaptic potentials of simple cells in cat visual cortex. J Neurosci. 1994 Nov;14(11 Pt 2):7130–7140. doi: 10.1523/JNEUROSCI.14-11-07130.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Pei X., Volgushev M., Vidyasagar T. R., Creutzfeldt O. D. Whole cell recording and conductance measurements in cat visual cortex in-vivo. Neuroreport. 1991 Aug;2(8):485–488. doi: 10.1097/00001756-199108000-00019. [DOI] [PubMed] [Google Scholar]
  20. Reid R. C., Soodak R. E., Shapley R. M. Directional selectivity and spatiotemporal structure of receptive fields of simple cells in cat striate cortex. J Neurophysiol. 1991 Aug;66(2):505–529. doi: 10.1152/jn.1991.66.2.505. [DOI] [PubMed] [Google Scholar]
  21. Sillito A. M., Jones H. E., Gerstein G. L., West D. C. Feature-linked synchronization of thalamic relay cell firing induced by feedback from the visual cortex. Nature. 1994 Jun 9;369(6480):479–482. doi: 10.1038/369479a0. [DOI] [PubMed] [Google Scholar]
  22. Sillito A. M. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J Physiol. 1975 Sep;250(2):305–329. doi: 10.1113/jphysiol.1975.sp011056. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Somers D. C., Nelson S. B., Sur M. An emergent model of orientation selectivity in cat visual cortical simple cells. J Neurosci. 1995 Aug;15(8):5448–5465. doi: 10.1523/JNEUROSCI.15-08-05448.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Tolhurst D. J., Dean A. F. Evaluation of a linear model of directional selectivity in simple cells of the cat's striate cortex. Vis Neurosci. 1991 May;6(5):421–428. doi: 10.1017/s0952523800001280. [DOI] [PubMed] [Google Scholar]
  25. Vidyasagar T. R. A model of striate response properties based on geniculate anisotropies. Biol Cybern. 1987;57(1-2):11–23. doi: 10.1007/BF00318712. [DOI] [PubMed] [Google Scholar]
  26. Vidyasagar T. R., Pei X., Volgushev M. Multiple mechanisms underlying the orientation selectivity of visual cortical neurones. Trends Neurosci. 1996 Jul;19(7):272–277. doi: 10.1016/S0166-2236(96)20027-X. [DOI] [PubMed] [Google Scholar]
  27. Vidyasagar T. R., Urbas J. V. Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Exp Brain Res. 1982;46(2):157–169. doi: 10.1007/BF00237172. [DOI] [PubMed] [Google Scholar]
  28. Volgushev M., Pei X., Vidyasagar T. R., Creutzfeldt O. D. Excitation and inhibition in orientation selectivity of cat visual cortex neurons revealed by whole-cell recordings in vivo. Vis Neurosci. 1993 Nov-Dec;10(6):1151–1155. doi: 10.1017/s0952523800010257. [DOI] [PubMed] [Google Scholar]
  29. Volgushev M., Pei X., Vidyasagar T. R., Creutzfeldt O. D. Postsynaptic potentials in cat visual cortex: dependence on polarization. Neuroreport. 1992 Aug;3(8):679–682. doi: 10.1097/00001756-199208000-00006. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES