Abstract
In the course of studies to map spatial frequency tuning of neurons in layers 2 and 3 of macaque striate cortex, we found that a high proportion (70%) of cells in the interblob regions responded poorly to full-field gratings, compared with responses to single bars, edges, or delimited gratings. This was most often due to side inhibition, in which increasing the number of cycles of a grating placed within the cell's receptive field causes progressive inhibition of response. Quantitative receptive-field mappings showed, however, that the inhibition can occur within the region activated by a bar, as well as beyond it. The inhibition appears to be orientation-selective, in that a surround grating was more effective at inhibiting the response to a center grating patch if it was of similar orientation. 2-Deoxyglucose experiments confirmed that side inhibition is very widespread in the interblobs of layers 2 and 3 and suggested that it is reduced or lacking in layers 4A through 6. Since layers 2 and 3 of striate cortex are the major source of cortical projections to area V2 and beyond, the prevalence of side stopping in these laminae has implications for theories of cortical visual function. Side-stopped interblob cells may be acting as "contour-pass filters" that filter out redundant information in textured or noisy surfaces, focusing subsequent form processing on contrasts corresponding to object boundaries.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- ATTNEAVE F. Some informational aspects of visual perception. Psychol Rev. 1954 May;61(3):183–193. doi: 10.1037/h0054663. [DOI] [PubMed] [Google Scholar]
- Albus K., Fries W. Inhibitory sidebands of complex receptive fields in the cats striate cortex. Vision Res. 1980;20(4):369–372. doi: 10.1016/0042-6989(80)90024-3. [DOI] [PubMed] [Google Scholar]
- Bishop P. O., Coombs J. S., Henry G. H. Receptive fields of simple cells in the cat striate cortex. J Physiol. 1973 May;231(1):31–60. doi: 10.1113/jphysiol.1973.sp010218. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blakemore C., Tobin E. A. Lateral inhibition between orientation detectors in the cat's visual cortex. Exp Brain Res. 1972;15(4):439–440. doi: 10.1007/BF00234129. [DOI] [PubMed] [Google Scholar]
- Bolz J., Gilbert C. D. Generation of end-inhibition in the visual cortex via interlaminar connections. 1986 Mar 27-Apr 2Nature. 320(6060):362–365. doi: 10.1038/320362a0. [DOI] [PubMed] [Google Scholar]
- Born R. T., Tootell R. B. Spatial frequency tuning of single units in macaque supragranular striate cortex. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):7066–7070. doi: 10.1073/pnas.88.16.7066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- De Valois R. L., Thorell L. G., Albrecht D. G. Periodicity of striate-cortex-cell receptive fields. J Opt Soc Am A. 1985 Jul;2(7):1115–1123. doi: 10.1364/josaa.2.001115. [DOI] [PubMed] [Google Scholar]
- Ferster D. A comparison of binocular depth mechanisms in areas 17 and 18 of the cat visual cortex. J Physiol. 1981 Feb;311:623–655. doi: 10.1113/jphysiol.1981.sp013608. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fries W., Albus K., Creutzfeldt O. D. Effects of interacting visual patterns on single cell responses in cats striate cortex. Vision Res. 1977;17(9):1001–1008. doi: 10.1016/0042-6989(77)90002-5. [DOI] [PubMed] [Google Scholar]
- Gaska J. P., Jacobson L. D., Pollen D. A. Response suppression by extending sine-wave gratings within the receptive fields of neurons in visual cortical area V3A of the macaque monkey. Vision Res. 1987;27(10):1687–1692. doi: 10.1016/0042-6989(87)90098-8. [DOI] [PubMed] [Google Scholar]
- 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]
- Gilbert C. D., Wiesel T. N. The influence of contextual stimuli on the orientation selectivity of cells in primary visual cortex of the cat. Vision Res. 1990;30(11):1689–1701. doi: 10.1016/0042-6989(90)90153-c. [DOI] [PubMed] [Google Scholar]
- Grossberg S., Mingolla E. Neural dynamics of form perception: boundary completion, illusory figures, and neon color spreading. Psychol Rev. 1985 Apr;92(2):173–211. [PubMed] [Google Scholar]
- Grossberg S., Mingolla E., Todorović D. A neural network architecture for preattentive vision. IEEE Trans Biomed Eng. 1989 Jan;36(1):65–84. doi: 10.1109/10.16450. [DOI] [PubMed] [Google Scholar]
- Jones B. H. Responses of single neurons in cat visual cortex to a simple and a more complex stimulus. Am J Physiol. 1970 Apr;218(4):1102–1107. doi: 10.1152/ajplegacy.1970.218.4.1102. [DOI] [PubMed] [Google Scholar]
- Maffei L., Fiorentini A. The unresponsive regions of visual cortical receptive fields. Vision Res. 1976;16(10):1131–1139. doi: 10.1016/0042-6989(76)90253-4. [DOI] [PubMed] [Google Scholar]
- 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]
- Nelson J. I., Frost B. J. Orientation-selective inhibition from beyond the classic visual receptive field. Brain Res. 1978 Jan 13;139(2):359–365. doi: 10.1016/0006-8993(78)90937-x. [DOI] [PubMed] [Google Scholar]
- Rockland K. S., Lund J. S. Intrinsic laminar lattice connections in primate visual cortex. J Comp Neurol. 1983 May 20;216(3):303–318. doi: 10.1002/cne.902160307. [DOI] [PubMed] [Google Scholar]
- Schiller P. H., Finlay B. L., Volman S. F. Quantitative studies of single-cell properties in monkey striate cortex. III. Spatial frequency. J Neurophysiol. 1976 Nov;39(6):1334–1351. doi: 10.1152/jn.1976.39.6.1334. [DOI] [PubMed] [Google Scholar]
- Tootell R. B., Hamilton S. L., Silverman M. S., Switkes E. Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. J Neurosci. 1988 May;8(5):1500–1530. doi: 10.1523/JNEUROSCI.08-05-01500.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tootell R. B., Silverman M. S., Hamilton S. L., Switkes E., De Valois R. L. Functional anatomy of macaque striate cortex. V. Spatial frequency. J Neurosci. 1988 May;8(5):1610–1624. doi: 10.1523/JNEUROSCI.08-05-01610.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ts'o D. Y., Gilbert C. D., Wiesel T. N. Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. J Neurosci. 1986 Apr;6(4):1160–1170. doi: 10.1523/JNEUROSCI.06-04-01160.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Westheimer G. Simultaneous orientation contrast for lines in the human fovea. Vision Res. 1990;30(11):1913–1921. doi: 10.1016/0042-6989(90)90167-j. [DOI] [PubMed] [Google Scholar]
- von der Heydt R., Peterhans E. Mechanisms of contour perception in monkey visual cortex. I. Lines of pattern discontinuity. J Neurosci. 1989 May;9(5):1731–1748. doi: 10.1523/JNEUROSCI.09-05-01731.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]