Skip to main content
NCBI home page
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 2000 Jan 29;355(1393):71–89. doi: 10.1098/rstb.2000.0550

Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor.

C C Hilgetag 1, M A O'Neill 1, M P Young 1
PMCID: PMC1692720  PMID: 10703045

Abstract

Neuroanatomists have described a large number of connections between the various structures of monkey and cat cortical sensory systems. Because of the complexity of the connection data, analysis is required to unravel what principles of organization they imply. To date, analysis of laminar origin and termination connection data to reveal hierarchical relationships between the cortical areas has been the most widely acknowledged approach. We programmed a network processor that searches for optimal hierarchical orderings of cortical areas given known hierarchical constraints and rules for their interpretation. For all cortical systems and all cost functions, the processor found a multitude of equally low-cost hierarchies. Laminar hierarchical constraints that are presently available in the anatomical literature were therefore insufficient to constrain a unique ordering for any of the sensory systems we analysed. Hierarchical orderings of the monkey visual system that have been widely reported, but which were derived by hand, were not among the optimal orderings. All the cortical systems we studied displayed a significant degree of hierarchical organization, and the anatomical constraints from the monkey visual and somato-motor systems were satisfied with very few constraint violations in the optimal hierarchies. The visual and somato-motor systems in that animal were therefore surprisingly strictly hierarchical. Most inconsistencies between the constraints and the hierarchical relationships in the optimal structures for the visual system were related to connections of area FST (fundus of superior temporal sulcus). We found that the hierarchical solutions could be further improved by assuming that FST consists of two areas, which differ in the nature of their projections. Indeed, we found that perfect hierarchical arrangements of the primate visual system, without any violation of anatomical constraints, could be obtained under two reasonable conditions, namely the subdivision of FST into two distinct areas, whose connectivity we predict, and the abolition of at least one of the less reliable rule constraints. Our analyses showed that the future collection of the same type of laminar constraints, or the inclusion of new hierarchical constraints from thalamocortical connections, will not resolve the problem of multiple optimal hierarchical representations for the primate visual system. Further data, however, may help to specify the relative ordering of some more areas. This indeterminacy of the visual hierarchy is in part due to the reported absence of some connections between cortical areas. These absences are consistent with limited cross-talk between differentiated processing streams in the system. Hence, hierarchical representation of the visual system is affected by, and must take into account, other organizational features, such as processing streams.

Full Text

The Full Text of this article is available as a PDF (352.0 KB).

Selected References

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

  1. Amir Y., Harel M., Malach R. Cortical hierarchy reflected in the organization of intrinsic connections in macaque monkey visual cortex. J Comp Neurol. 1993 Aug 1;334(1):19–46. doi: 10.1002/cne.903340103. [DOI] [PubMed] [Google Scholar]
  2. Barbas H. Pattern in the laminar origin of corticocortical connections. J Comp Neurol. 1986 Oct 15;252(3):415–422. doi: 10.1002/cne.902520310. [DOI] [PubMed] [Google Scholar]
  3. Barbas H., Rempel-Clower N. Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex. 1997 Oct-Nov;7(7):635–646. doi: 10.1093/cercor/7.7.635. [DOI] [PubMed] [Google Scholar]
  4. Boussaoud D., Ungerleider L. G., Desimone R. Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol. 1990 Jun 15;296(3):462–495. doi: 10.1002/cne.902960311. [DOI] [PubMed] [Google Scholar]
  5. Clarke S. Modular organization of human extrastriate visual cortex: evidence from cytochrome oxidase pattern in normal and macular degeneration cases. Eur J Neurosci. 1994 May 1;6(5):725–736. doi: 10.1111/j.1460-9568.1994.tb00984.x. [DOI] [PubMed] [Google Scholar]
  6. Coogan T. A., Burkhalter A. Hierarchical organization of areas in rat visual cortex. J Neurosci. 1993 Sep;13(9):3749–3772. doi: 10.1523/JNEUROSCI.13-09-03749.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cusick C. G., Seltzer B., Cola M., Griggs E. Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: evidence for subdivisions of superior temporal polysensory cortex. J Comp Neurol. 1995 Sep 25;360(3):513–535. doi: 10.1002/cne.903600312. [DOI] [PubMed] [Google Scholar]
  8. Dinse H. R., Krüger K. The timing of processing along the visual pathway in the cat. Neuroreport. 1994 Apr 14;5(8):893–897. doi: 10.1097/00001756-199404000-00010. [DOI] [PubMed] [Google Scholar]
  9. Elston G. N., Rosa M. G. Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cereb Cortex. 1998 Apr-May;8(3):278–294. doi: 10.1093/cercor/8.3.278. [DOI] [PubMed] [Google Scholar]
  10. Elston G. N., Rosa M. G. The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex. 1997 Jul-Aug;7(5):432–452. doi: 10.1093/cercor/7.5.432. [DOI] [PubMed] [Google Scholar]
  11. 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]
  12. Hilgetag C. C., O'Neill M. A., Young M. P. Indeterminate organization of the visual system. Science. 1996 Feb 9;271(5250):776–777. doi: 10.1126/science.271.5250.776. [DOI] [PubMed] [Google Scholar]
  13. Kaas J. H., Morel A. Connections of visual areas of the upper temporal lobe of owl monkeys: the MT crescent and dorsal and ventral subdivisions of FST. J Neurosci. 1993 Feb;13(2):534–546. doi: 10.1523/JNEUROSCI.13-02-00534.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Maunsell J. H., van Essen D. C. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci. 1983 Dec;3(12):2563–2586. doi: 10.1523/JNEUROSCI.03-12-02563.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Nakamura H., Gattass R., Desimone R., Ungerleider L. G. The modular organization of projections from areas V1 and V2 to areas V4 and TEO in macaques. J Neurosci. 1993 Sep;13(9):3681–3691. doi: 10.1523/JNEUROSCI.13-09-03681.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Olavarria J. F., Abel P. L. The distribution of callosal connections correlates with the pattern of cytochrome oxidase stripes in visual area V2 of macaque monkeys. Cereb Cortex. 1996 Jul-Aug;6(4):631–639. doi: 10.1093/cercor/6.4.631. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Rockland K. S. Two types of corticopulvinar terminations: round (type 2) and elongate (type 1). J Comp Neurol. 1996 Apr 22;368(1):57–87. doi: 10.1002/(SICI)1096-9861(19960422)368:1<57::AID-CNE5>3.0.CO;2-J. [DOI] [PubMed] [Google Scholar]
  19. Scannell J. W., Blakemore C., Young M. P. Analysis of connectivity in the cat cerebral cortex. J Neurosci. 1995 Feb;15(2):1463–1483. doi: 10.1523/JNEUROSCI.15-02-01463.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Scannell J. W., Burns G. A., Hilgetag C. C., O'Neil M. A., Young M. P. The connectional organization of the cortico-thalamic system of the cat. Cereb Cortex. 1999 Apr-May;9(3):277–299. doi: 10.1093/cercor/9.3.277. [DOI] [PubMed] [Google Scholar]
  21. Schmolesky M. T., Wang Y., Hanes D. P., Thompson K. G., Leutgeb S., Schall J. D., Leventhal A. G. Signal timing across the macaque visual system. J Neurophysiol. 1998 Jun;79(6):3272–3278. doi: 10.1152/jn.1998.79.6.3272. [DOI] [PubMed] [Google Scholar]
  22. Schroeder C. E., Mehta A. D., Givre S. J. A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. Cereb Cortex. 1998 Oct-Nov;8(7):575–592. doi: 10.1093/cercor/8.7.575. [DOI] [PubMed] [Google Scholar]
  23. Van Essen D. C., Anderson C. H., Felleman D. J. Information processing in the primate visual system: an integrated systems perspective. Science. 1992 Jan 24;255(5043):419–423. doi: 10.1126/science.1734518. [DOI] [PubMed] [Google Scholar]
  24. Van Essen D. C., Felleman D. J. On hierarchies: response to Hilgetag et al. Science. 1996 Feb 9;271(5250):777–777. [PubMed] [Google Scholar]
  25. Webster M. J., Bachevalier J., Ungerleider L. G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex. 1994 Sep-Oct;4(5):470–483. doi: 10.1093/cercor/4.5.470. [DOI] [PubMed] [Google Scholar]
  26. Young M. P. Objective analysis of the topological organization of the primate cortical visual system. Nature. 1992 Jul 9;358(6382):152–155. doi: 10.1038/358152a0. [DOI] [PubMed] [Google Scholar]
  27. Young M. P., Scannell J. W., O'Neill M. A., Hilgetag C. C., Burns G., Blakemore C. Non-metric multidimensional scaling in the analysis of neuroanatomical connection data and the organization of the primate cortical visual system. Philos Trans R Soc Lond B Biol Sci. 1995 May 30;348(1325):281–308. doi: 10.1098/rstb.1995.0069. [DOI] [PubMed] [Google Scholar]

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

RESOURCES