Abstract
The relationships between cytochrome oxidase blobs, ocular-dominance columns, and iso-orientation domains, subsystems underlying visual perception, were explored in primary visual cortex of macaque monkey. High-resolution maps of these three subsystems were acquired. Optical imaging based on activity-dependent intrinsic signals revealed that the most prominent organizational feature of orientation preference was a radial arrangement, forming a pinwheel-like structure surrounding a singularity point. More than 80% of these pinwheels were centered along the midline of ocular-dominance columns. The iso-orientation contours of adjacent pinwheels crossed borders of ocular-dominance columns at approximately right angles. Pinwheels with the same or opposite directions of orientation-preference change were smoothly connected with each other. On the average, all orientations were equally represented. In exactly the same cortical area, the cytochrome oxidase blobs, thought to be involved in color processing, were also mapped, using cytochrome oxidase histology. Like the centers of pinwheels, the centers of blobs also lie along the midline of ocular-dominance columns. However, the centers of pinwheels did not coincide with the centers of blobs; these two subsystems are spatially independent. "Hypercolumn" modules, each including two complete pinwheels in two adjacent columns of complementary ocularity, as well as portions of a few blobs, were frequently found but did not seem to be the primary unit of cortical organization. An alternative to hypercolumns is proposed.
Full text
PDF




Images in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Blasdel G. G. Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. J Neurosci. 1992 Aug;12(8):3115–3138. doi: 10.1523/JNEUROSCI.12-08-03115.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blasdel G. G. Orientation selectivity, preference, and continuity in monkey striate cortex. J Neurosci. 1992 Aug;12(8):3139–3161. doi: 10.1523/JNEUROSCI.12-08-03139.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Blasdel G. G., Salama G. Voltage-sensitive dyes reveal a modular organization in monkey striate cortex. Nature. 1986 Jun 5;321(6070):579–585. doi: 10.1038/321579a0. [DOI] [PubMed] [Google Scholar]
- Bonhoeffer T., Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature. 1991 Oct 3;353(6343):429–431. doi: 10.1038/353429a0. [DOI] [PubMed] [Google Scholar]
- Braitenberg V., Braitenberg C. Geometry of orientation columns in the visual cortex. Biol Cybern. 1979 Aug 1;33(3):179–186. doi: 10.1007/BF00337296. [DOI] [PubMed] [Google Scholar]
- CHANCE B., COHEN P., JOBSIS F., SCHOENER B. Intracellular oxidation-reduction states in vivo. Science. 1962 Aug 17;137(3529):499–508. doi: 10.1126/science.137.3529.499. [DOI] [PubMed] [Google Scholar]
- Cohen L. B., Salzberg B. M., Davila H. V., Ross W. N., Landowne D., Waggoner A. S., Wang C. H. Changes in axon fluorescence during activity: molecular probes of membrane potential. J Membr Biol. 1974;19(1):1–36. doi: 10.1007/BF01869968. [DOI] [PubMed] [Google Scholar]
- Frostig R. D., Lieke E. E., Ts'o D. Y., Grinvald A. Cortical functional architecture and local coupling between neuronal activity and the microcirculation revealed by in vivo high-resolution optical imaging of intrinsic signals. Proc Natl Acad Sci U S A. 1990 Aug;87(16):6082–6086. doi: 10.1073/pnas.87.16.6082. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grinvald A., Anglister L., Freeman J. A., Hildesheim R., Manker A. Real-time optical imaging of naturally evoked electrical activity in intact frog brain. 1984 Apr 26-May 2Nature. 308(5962):848–850. doi: 10.1038/308848a0. [DOI] [PubMed] [Google Scholar]
- Grinvald A., Frostig R. D., Lieke E., Hildesheim R. Optical imaging of neuronal activity. Physiol Rev. 1988 Oct;68(4):1285–1366. doi: 10.1152/physrev.1988.68.4.1285. [DOI] [PubMed] [Google Scholar]
- Grinvald A., Frostig R. D., Siegel R. M., Bartfeld E. High-resolution optical imaging of functional brain architecture in the awake monkey. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11559–11563. doi: 10.1073/pnas.88.24.11559. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grinvald A., Lieke E., Frostig R. D., Gilbert C. D., Wiesel T. N. Functional architecture of cortex revealed by optical imaging of intrinsic signals. 1986 Nov 27-Dec 3Nature. 324(6095):361–364. doi: 10.1038/324361a0. [DOI] [PubMed] [Google Scholar]
- Grinvald A., Manker A., Segal M. Visualization of the spread of electrical activity in rat hippocampal slices by voltage-sensitive optical probes. J Physiol. 1982 Dec;333:269–291. doi: 10.1113/jphysiol.1982.sp014453. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grinvald A., Salzberg B. M., Cohen L. B. Simultaneous recording from several neurones in an invertebrate central nervous system. Nature. 1977 Jul 14;268(5616):140–142. doi: 10.1038/268140a0. [DOI] [PubMed] [Google Scholar]
- Götz K. G. Cortical templates for the self-organization of orientation-specific d- and l-hypercolumns in monkeys and cats. Biol Cybern. 1988;58(4):213–223. doi: 10.1007/BF00364127. [DOI] [PubMed] [Google Scholar]
- HILL D. K., KEYNES R. D. Opacity changes in stimulated nerve. J Physiol. 1949 May;108(3):278–281. [PubMed] [Google Scholar]
- Horton J. C., Hubel D. H. Regular patchy distribution of cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature. 1981 Aug 20;292(5825):762–764. doi: 10.1038/292762a0. [DOI] [PubMed] [Google Scholar]
- Hubel D. H., Wiesel T. N. Ferrier lecture. Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci. 1977 Jul 28;198(1130):1–59. doi: 10.1098/rspb.1977.0085. [DOI] [PubMed] [Google Scholar]
- Hubel D. H., Wiesel T. N. Receptive fields and functional architecture of monkey striate cortex. J Physiol. 1968 Mar;195(1):215–243. doi: 10.1113/jphysiol.1968.sp008455. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hubel D. H., Wiesel T. N. Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol. 1974 Dec 1;158(3):267–293. doi: 10.1002/cne.901580304. [DOI] [PubMed] [Google Scholar]
- Hubel D. H., Wiesel T. N., Stryker M. P. Anatomical demonstration of orientation columns in macaque monkey. J Comp Neurol. 1978 Feb 1;177(3):361–380. doi: 10.1002/cne.901770302. [DOI] [PubMed] [Google Scholar]
- Jöbsis F. F., Keizer J. H., LaManna J. C., Rosenthal M. Reflectance spectrophotometry of cytochrome aa3 in vivo. J Appl Physiol Respir Environ Exerc Physiol. 1977 Nov;43(5):858–872. doi: 10.1152/jappl.1977.43.5.858. [DOI] [PubMed] [Google Scholar]
- LeVay S., Hubel D. H., Wiesel T. N. The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. J Comp Neurol. 1975 Feb 15;159(4):559–576. doi: 10.1002/cne.901590408. [DOI] [PubMed] [Google Scholar]
- Linsker R. From basic network principles to neural architecture: emergence of orientation columns. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8779–8783. doi: 10.1073/pnas.83.22.8779. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Livingstone M. S., Hubel D. H. Anatomy and physiology of a color system in the primate visual cortex. J Neurosci. 1984 Jan;4(1):309–356. doi: 10.1523/JNEUROSCI.04-01-00309.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- MOUNTCASTLE V. B. Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol. 1957 Jul;20(4):408–434. doi: 10.1152/jn.1957.20.4.408. [DOI] [PubMed] [Google Scholar]
- Orbach H. S., Cohen L. B., Grinvald A. Optical mapping of electrical activity in rat somatosensory and visual cortex. J Neurosci. 1985 Jul;5(7):1886–1895. doi: 10.1523/JNEUROSCI.05-07-01886.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Orbach H. S., Cohen L. B. Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system. J Neurosci. 1983 Nov;3(11):2251–2262. doi: 10.1523/JNEUROSCI.03-11-02251.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ratzlaff E. H., Grinvald A. A tandem-lens epifluorescence macroscope: hundred-fold brightness advantage for wide-field imaging. J Neurosci Methods. 1991 Feb;36(2-3):127–137. doi: 10.1016/0165-0270(91)90038-2. [DOI] [PubMed] [Google Scholar]
- Salzberg B. M., Davila H. V., Cohen L. B. Optical recording of impulses in individual neurones of an invertebrate central nervous system. Nature. 1973 Dec 21;246(5434):508–509. doi: 10.1038/246508a0. [DOI] [PubMed] [Google Scholar]
- Swindale N. V. A model for the formation of orientation columns. Proc R Soc Lond B Biol Sci. 1982 May 22;215(1199):211–230. doi: 10.1098/rspb.1982.0038. [DOI] [PubMed] [Google Scholar]
- Swindale N. V., Matsubara J. A., Cynader M. S. Surface organization of orientation and direction selectivity in cat area 18. J Neurosci. 1987 May;7(5):1414–1427. doi: 10.1523/JNEUROSCI.07-05-01414.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tasaki I., Watanabe A., Sandlin R., Carnay L. Changes in fluorescence, turbidity, and birefringence associated with nerve excitation. Proc Natl Acad Sci U S A. 1968 Nov;61(3):883–888. doi: 10.1073/pnas.61.3.883. [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., Frostig R. D., Lieke E. E., Grinvald A. Functional organization of primate visual cortex revealed by high resolution optical imaging. Science. 1990 Jul 27;249(4967):417–420. doi: 10.1126/science.2165630. [DOI] [PubMed] [Google Scholar]
- Ts'o D. Y., Gilbert C. D. The organization of chromatic and spatial interactions in the primate striate cortex. J Neurosci. 1988 May;8(5):1712–1727. doi: 10.1523/JNEUROSCI.08-05-01712.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Waggoner A. S., Grinvald A. Mechanisms of rapid optical changes of potential sensitive dyes. Ann N Y Acad Sci. 1977 Dec 30;303:217–241. [PubMed] [Google Scholar]