Skip to main content
NCBI home page
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
. 1995 Apr 25;92(9):3844–3848. doi: 10.1073/pnas.92.9.3844

Theory of orientation tuning in visual cortex.

R Ben-Yishai 1, R L Bar-Or 1, H Sompolinsky 1
PMCID: PMC42058  PMID: 7731993

Abstract

The role of intrinsic cortical connections in processing sensory input and in generating behavioral output is poorly understood. We have examined this issue in the context of the tuning of neuronal responses in cortex to the orientation of a visual stimulus. We analytically study a simple network model that incorporates both orientation-selective input from the lateral geniculate nucleus and orientation-specific cortical interactions. Depending on the model parameters, the network exhibits orientation selectivity that originates from within the cortex, by a symmetry-breaking mechanism. In this case, the width of the orientation tuning can be sharp even if the lateral geniculate nucleus inputs are only weakly anisotropic. By using our model, several experimental consequences of this cortical mechanism of orientation tuning are derived. The tuning width is relatively independent of the contrast and angular anisotropy of the visual stimulus. The transient population response to changing of the stimulus orientation exhibits a slow "virtual rotation." Neuronal cross-correlations exhibit long time tails, the sign of which depends on the preferred orientations of the cells and the stimulus orientation.

Full text

PDF
3844

Images in this article

3847Fig. 3
on p.3847

Selected References

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

  1. Ahmed B., Anderson J. C., Douglas R. J., Martin K. A., Nelson J. C. Polyneuronal innervation of spiny stellate neurons in cat visual cortex. J Comp Neurol. 1994 Mar 1;341(1):39–49. doi: 10.1002/cne.903410105. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Douglas R. J., Martin K. A., Whitteridge D. An intracellular analysis of the visual responses of neurones in cat visual cortex. J Physiol. 1991;440:659–696. doi: 10.1113/jphysiol.1991.sp018730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Fetz E. E., Shupe L. E. Measuring synaptic interactions. Science. 1994 Mar 4;263(5151):1295–1297. doi: 10.1126/science.8122116. [DOI] [PubMed] [Google Scholar]
  6. Georgopoulos A. P., Massey J. T. Cognitive spatial-motor processes. 1. The making of movements at various angles from a stimulus direction. Exp Brain Res. 1987;65(2):361–370. doi: 10.1007/BF00236309. [DOI] [PubMed] [Google Scholar]
  7. Georgopoulos A. P., Taira M., Lukashin A. Cognitive neurophysiology of the motor cortex. Science. 1993 Apr 2;260(5104):47–52. doi: 10.1126/science.8465199. [DOI] [PubMed] [Google Scholar]
  8. Ginzburg I, I, Sompolinsky H. Theory of correlations in stochastic neural networks. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics. 1994 Oct;50(4):3171–3191. doi: 10.1103/physreve.50.3171. [DOI] [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. Hata Y., Tsumoto T., Sato H., Hagihara K., Tamura H. Inhibition contributes to orientation selectivity in visual cortex of cat. Nature. 1988 Oct 27;335(6193):815–817. doi: 10.1038/335815a0. [DOI] [PubMed] [Google Scholar]
  11. Lukashin A. V., Georgopoulos A. P. A dynamical neural network model for motor cortical activity during movement: population coding of movement trajectories. Biol Cybern. 1993;69(5-6):517–524. [PubMed] [Google Scholar]
  12. 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]
  13. Shepard R. N., Metzler J. Mental rotation of three-dimensional objects. Science. 1971 Feb 19;171(3972):701–703. doi: 10.1126/science.171.3972.701. [DOI] [PubMed] [Google Scholar]
  14. Sillito A. M., Kemp J. A., Milson J. A., Berardi N. A re-evaluation of the mechanisms underlying simple cell orientation selectivity. Brain Res. 1980 Aug 4;194(2):517–520. doi: 10.1016/0006-8993(80)91234-2. [DOI] [PubMed] [Google Scholar]
  15. Skottun B. C., Bradley A., Sclar G., Ohzawa I., Freeman R. D. The effects of contrast on visual orientation and spatial frequency discrimination: a comparison of single cells and behavior. J Neurophysiol. 1987 Mar;57(3):773–786. doi: 10.1152/jn.1987.57.3.773. [DOI] [PubMed] [Google Scholar]
  16. Tolhurst D. J., Movshon J. A., Thompson I. D. The dependence of response amplitude and variance of cat visual cortical neurones on stimulus contrast. Exp Brain Res. 1981;41(3-4):414–419. doi: 10.1007/BF00238900. [DOI] [PubMed] [Google Scholar]
  17. Tsumoto T., Eckart W., Creutzfeldt O. D. Modification of orientation sensitivity of cat visual cortex neurons by removal of GABA-mediated inhibition. Exp Brain Res. 1979 Jan 15;34(2):351–363. doi: 10.1007/BF00235678. [DOI] [PubMed] [Google Scholar]
  18. Vaadia E., Haalman I., Abeles M., Bergman H., Prut Y., Slovin H., Aertsen A. Dynamics of neuronal interactions in monkey cortex in relation to behavioural events. Nature. 1995 Feb 9;373(6514):515–518. doi: 10.1038/373515a0. [DOI] [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