Skip to main content
PMC home page
Proceedings of the Royal Society B: Biological Sciences logoLink to Proceedings of the Royal Society B: Biological Sciences
. 1998 Jun 7;265(1400):1037–1044. doi: 10.1098/rspb.1998.0396

Extrastriate feedback to primary visual cortex in primates: a quantitative analysis of connectivity.

J M Budd 1
PMCID: PMC1689163  PMID: 9675911

Abstract

Knowledge-based or top-down influences on primary visual cortex (area V1) are believed to originate from information conveyed by extrastriate feedback axon connections. Understanding how this information is communicated to area V1 neurons relies in part on elucidating the quantitative as well as the qualitative nature of extrastriate pathway connectivity. A quantitative analysis of the connectivity based on anatomical data regarding the feedback pathway from extrastriate area V2 to area V1 in macaque monkey suggests (i) a total of around ten million or more area V2 axons project to area V1; (ii) the mean number of synaptic inputs from area V2 per upper-layer pyramidal cell in area V1 is less than 6% of all excitatory inputs; and (iii) the mean degree of convergence of area V2 afferents may be high, perhaps more than 100 afferent axons per cell. These results are consistent with empirical observations of the density of radial myelinated axons present in the upper layers in macaque area V1 and the proportion of excitatory extrastriate feedback synaptic inputs onto upper-layer neurons in rat visual cortex. Thus, in primate area V1, extrastriate feedback synapses onto upper-layer cells may, like geniculocortical afferent synapses onto layer IVC neurons, form only a small percentage of the total excitatory synaptic input.

Full Text

The Full Text of this article is available as a PDF (178.1 KB).

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. Amitai Y., Friedman A., Connors B. W., Gutnick M. J. Regenerative activity in apical dendrites of pyramidal cells in neocortex. Cereb Cortex. 1993 Jan-Feb;3(1):26–38. doi: 10.1093/cercor/3.1.26. [DOI] [PubMed] [Google Scholar]
  3. Anderson J. C., Martin K. A., Whitteridge D. Form, function, and intracortical projections of neurons in the striate cortex of the monkey Macacus nemestrinus. Cereb Cortex. 1993 Sep-Oct;3(5):412–420. doi: 10.1093/cercor/3.5.412. [DOI] [PubMed] [Google Scholar]
  4. Barone P., Dehay C., Berland M., Bullier J., Kennedy H. Developmental remodeling of primate visual cortical pathways. Cereb Cortex. 1995 Jan-Feb;5(1):22–38. doi: 10.1093/cercor/5.1.22. [DOI] [PubMed] [Google Scholar]
  5. Beaulieu C., Kisvarday Z., Somogyi P., Cynader M., Cowey A. Quantitative distribution of GABA-immunopositive and -immunonegative neurons and synapses in the monkey striate cortex (area 17). Cereb Cortex. 1992 Jul-Aug;2(4):295–309. doi: 10.1093/cercor/2.4.295. [DOI] [PubMed] [Google Scholar]
  6. Bernander O., Douglas R. J., Martin K. A., Koch C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci U S A. 1991 Dec 15;88(24):11569–11573. doi: 10.1073/pnas.88.24.11569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Blasdel G. G., Lund J. S. Termination of afferent axons in macaque striate cortex. J Neurosci. 1983 Jul;3(7):1389–1413. doi: 10.1523/JNEUROSCI.03-07-01389.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Celebrini S., Thorpe S., Trotter Y., Imbert M. Dynamics of orientation coding in area V1 of the awake primate. Vis Neurosci. 1993 Sep-Oct;10(5):811–825. doi: 10.1017/s0952523800006052. [DOI] [PubMed] [Google Scholar]
  9. Contreras D., Destexhe A., Sejnowski T. J., Steriade M. Control of spatiotemporal coherence of a thalamic oscillation by corticothalamic feedback. Science. 1996 Nov 1;274(5288):771–774. doi: 10.1126/science.274.5288.771. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Essen D. C., Zeki S. M. The topographic organization of rhesus monkey prestriate cortex. J Physiol. 1978 Apr;277:193–226. doi: 10.1113/jphysiol.1978.sp012269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Felleman D. J., Van Essen D. C. Distributed hierarchical processing in the primate cerebral cortex. Cereb Cortex. 1991 Jan-Feb;1(1):1–47. doi: 10.1093/cercor/1.1.1-a. [DOI] [PubMed] [Google Scholar]
  13. Freund T. F., Martin K. A., Soltesz I., Somogyi P., Whitteridge D. Arborisation pattern and postsynaptic targets of physiologically identified thalamocortical afferents in striate cortex of the macaque monkey. J Comp Neurol. 1989 Nov 8;289(2):315–336. doi: 10.1002/cne.902890211. [DOI] [PubMed] [Google Scholar]
  14. Johnson R. R., Burkhalter A. A polysynaptic feedback circuit in rat visual cortex. J Neurosci. 1997 Sep 15;17(18):7129–7140. doi: 10.1523/JNEUROSCI.17-18-07129.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Johnson R. R., Burkhalter A. Microcircuitry of forward and feedback connections within rat visual cortex. J Comp Neurol. 1996 May 6;368(3):383–398. doi: 10.1002/(SICI)1096-9861(19960506)368:3<383::AID-CNE5>3.0.CO;2-1. [DOI] [PubMed] [Google Scholar]
  16. Kennedy H., Bullier J. A double-labeling investigation of the afferent connectivity to cortical areas V1 and V2 of the macaque monkey. J Neurosci. 1985 Oct;5(10):2815–2830. doi: 10.1523/JNEUROSCI.05-10-02815.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Levitt J. B., Kiper D. C., Movshon J. A. Receptive fields and functional architecture of macaque V2. J Neurophysiol. 1994 Jun;71(6):2517–2542. doi: 10.1152/jn.1994.71.6.2517. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Markram H., Lübke J., Frotscher M., Roth A., Sakmann B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J Physiol. 1997 Apr 15;500(Pt 2):409–440. doi: 10.1113/jphysiol.1997.sp022031. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. McGuire B. A., Gilbert C. D., Rivlin P. K., Wiesel T. N. Targets of horizontal connections in macaque primary visual cortex. J Comp Neurol. 1991 Mar 15;305(3):370–392. doi: 10.1002/cne.903050303. [DOI] [PubMed] [Google Scholar]
  21. Motter B. C. Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli. J Neurophysiol. 1993 Sep;70(3):909–919. doi: 10.1152/jn.1993.70.3.909. [DOI] [PubMed] [Google Scholar]
  22. Mumford D. On the computational architecture of the neocortex. II. The role of cortico-cortical loops. Biol Cybern. 1992;66(3):241–251. doi: 10.1007/BF00198477. [DOI] [PubMed] [Google Scholar]
  23. Nowak L. G., Munk M. H., Nelson J. I., James A. C., Bullier J. Structural basis of cortical synchronization. I. Three types of interhemispheric coupling. J Neurophysiol. 1995 Dec;74(6):2379–2400. doi: 10.1152/jn.1995.74.6.2379. [DOI] [PubMed] [Google Scholar]
  24. Perkel D. J., Bullier J., Kennedy H. Topography of the afferent connectivity of area 17 in the macaque monkey: a double-labelling study. J Comp Neurol. 1986 Nov 15;253(3):374–402. doi: 10.1002/cne.902530307. [DOI] [PubMed] [Google Scholar]
  25. Peters A., Payne B. R., Budd J. A numerical analysis of the geniculocortical input to striate cortex in the monkey. Cereb Cortex. 1994 May-Jun;4(3):215–229. doi: 10.1093/cercor/4.3.215. [DOI] [PubMed] [Google Scholar]
  26. Peters A., Payne B. R. Numerical relationships between geniculocortical afferents and pyramidal cell modules in cat primary visual cortex. Cereb Cortex. 1993 Jan-Feb;3(1):69–78. doi: 10.1093/cercor/3.1.69. [DOI] [PubMed] [Google Scholar]
  27. Peters A., Sethares C. Myelinated axons and the pyramidal cell modules in monkey primary visual cortex. J Comp Neurol. 1996 Feb 5;365(2):232–255. doi: 10.1002/(SICI)1096-9861(19960205)365:2<232::AID-CNE3>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  28. Peters A., Sethares C. Organization of pyramidal neurons in area 17 of monkey visual cortex. J Comp Neurol. 1991 Apr 1;306(1):1–23. doi: 10.1002/cne.903060102. [DOI] [PubMed] [Google Scholar]
  29. Rockland K. S., Pandya D. N. Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Res. 1979 Dec 21;179(1):3–20. doi: 10.1016/0006-8993(79)90485-2. [DOI] [PubMed] [Google Scholar]
  30. Rockland K. S., Virga A. Terminal arbors of individual "feedback" axons projecting from area V2 to V1 in the macaque monkey: a study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. J Comp Neurol. 1989 Jul 1;285(1):54–72. doi: 10.1002/cne.902850106. [DOI] [PubMed] [Google Scholar]
  31. Salin P. A., Bullier J. Corticocortical connections in the visual system: structure and function. Physiol Rev. 1995 Jan;75(1):107–154. doi: 10.1152/physrev.1995.75.1.107. [DOI] [PubMed] [Google Scholar]
  32. Sandell J. H., Schiller P. H. Effect of cooling area 18 on striate cortex cells in the squirrel monkey. J Neurophysiol. 1982 Jul;48(1):38–48. doi: 10.1152/jn.1982.48.1.38. [DOI] [PubMed] [Google Scholar]
  33. Sawatari A., Callaway E. M. Convergence of magno- and parvocellular pathways in layer 4B of macaque primary visual cortex. Nature. 1996 Apr 4;380(6573):442–446. doi: 10.1038/380442a0. [DOI] [PubMed] [Google Scholar]
  34. Shao Z., Burkhalter A. Different balance of excitation and inhibition in forward and feedback circuits of rat visual cortex. J Neurosci. 1996 Nov 15;16(22):7353–7365. doi: 10.1523/JNEUROSCI.16-22-07353.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Shipp S., Zeki S. The Organization of Connections between Areas V5 and V1 in Macaque Monkey Visual Cortex. Eur J Neurosci. 1989;1(4):309–332. doi: 10.1111/j.1460-9568.1989.tb00798.x. [DOI] [PubMed] [Google Scholar]
  36. Ullman S. Sequence seeking and counter streams: a computational model for bidirectional information flow in the visual cortex. Cereb Cortex. 1995 Jan-Feb;5(1):1–11. doi: 10.1093/cercor/5.1.1. [DOI] [PubMed] [Google Scholar]
  37. Weller R. E., Kaas J. H. Retinotopic patterns of connections of area 17 with visual areas V-II and MT in macaque monkeys. J Comp Neurol. 1983 Nov 1;220(3):253–279. doi: 10.1002/cne.902200302. [DOI] [PubMed] [Google Scholar]
  38. Zeki S. M. Uniformity and diversity of structure and function in rhesus monkey prestriate visual cortex. J Physiol. 1978 Apr;277:273–290. doi: 10.1113/jphysiol.1978.sp012272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Zipser K., Lamme V. A., Schiller P. H. Contextual modulation in primary visual cortex. J Neurosci. 1996 Nov 15;16(22):7376–7389. doi: 10.1523/JNEUROSCI.16-22-07376.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society

RESOURCES