Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1997 Oct 29;352(1360):1429–1436. doi: 10.1098/rstb.1997.0129

From visual affordances in monkey parietal cortex to hippocampo-parietal interactions underlying rat navigation.

M A Arbib 1
PMCID: PMC1692057  PMID: 9368931

Abstract

This paper explores the hypothesis that various subregions (but by no means all) of the posterior parietal cortex are specialized to process visual information to extract a variety of affordances for behaviour. Two biologically based models of regions of the posterior parietal cortex of the monkey are introduced. The model of the lateral intraparietal area (LIP) emphasizes its roles in dynamic remapping of the representation of targets during a double saccade task, and in combining stored, updated input with current visual input. The model of the anterior intraparietal area (AIP) addresses parietal-premotor interactions involved in grasping, and analyses the interaction between the AIP and premotor area F5. The model represents the role of other intraparietal areas working in concert with the inferotemporal cortex as well as with corollary discharge from F5 to provide and augment the affordance information in the AIP, and suggests how various constraints may resolve the action opportunities provided by multiple affordances. Finally, a systems-level model of hippocampo parietal interactions underlying rat navigation is developed, motivated by the monkey data used in developing the above two models as well as by data on neurones in the posterior parietal cortex of the monkey that are sensitive to visual motion. The formal similarity between dynamic remapping (primate saccades) and path integration (rat navigation) is noted, and certain available data on rat posterior parietal cortex in terms of affordances for locomotion are explained. The utility of further modelling, linking the World Graph model of cognitive maps for motivated behaviour with hippocampal-parietal interactions involved in navigation, is also suggested. These models demonstrate that posterior parietal cortex is not only itself a network of interacting subsystems, but functions through cooperative computation with many other brain regions.

Full Text

The Full Text of this article is available as a PDF (157.5 KB).

Selected References

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

  1. Baizer J. S., Ungerleider L. G., Desimone R. Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci. 1991 Jan;11(1):168–190. doi: 10.1523/JNEUROSCI.11-01-00168.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Castiello U., Paulignan Y., Jeannerod M. Temporal dissociation of motor responses and subjective awareness. A study in normal subjects. Brain. 1991 Dec;114(Pt 6):2639–2655. doi: 10.1093/brain/114.6.2639. [DOI] [PubMed] [Google Scholar]
  3. Chen L. L., Lin L. H., Barnes C. A., McNaughton B. L. Head-direction cells in the rat posterior cortex. II. Contributions of visual and ideothetic information to the directional firing. Exp Brain Res. 1994;101(1):24–34. doi: 10.1007/BF00243213. [DOI] [PubMed] [Google Scholar]
  4. Chen L. L., Lin L. H., Green E. J., Barnes C. A., McNaughton B. L. Head-direction cells in the rat posterior cortex. I. Anatomical distribution and behavioral modulation. Exp Brain Res. 1994;101(1):8–23. doi: 10.1007/BF00243212. [DOI] [PubMed] [Google Scholar]
  5. Colby C. L., Duhamel J. R., Goldberg M. E. Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol. 1993 Mar;69(3):902–914. doi: 10.1152/jn.1993.69.3.902. [DOI] [PubMed] [Google Scholar]
  6. Dominey P. F., Arbib M. A. A cortico-subcortical model for generation of spatially accurate sequential saccades. Cereb Cortex. 1992 Mar-Apr;2(2):153–175. doi: 10.1093/cercor/2.2.153. [DOI] [PubMed] [Google Scholar]
  7. Droulez J., Berthoz A. A neural network model of sensoritopic maps with predictive short-term memory properties. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9653–9657. doi: 10.1073/pnas.88.21.9653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Eichenbaum H., Kuperstein M., Fagan A., Nagode J. Cue-sampling and goal-approach correlates of hippocampal unit activity in rats performing an odor-discrimination task. J Neurosci. 1987 Mar;7(3):716–732. doi: 10.1523/JNEUROSCI.07-03-00716.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Gnadt J. W., Andersen R. A. Memory related motor planning activity in posterior parietal cortex of macaque. Exp Brain Res. 1988;70(1):216–220. doi: 10.1007/BF00271862. [DOI] [PubMed] [Google Scholar]
  10. Goldberg M. E., Bruce C. J. Primate frontal eye fields. III. Maintenance of a spatially accurate saccade signal. J Neurophysiol. 1990 Aug;64(2):489–508. doi: 10.1152/jn.1990.64.2.489. [DOI] [PubMed] [Google Scholar]
  11. Kase C. S., Troncoso J. F., Court J. E., Tapia J. F., Mohr J. P. Global spatial disorientation. Clinico-pathologic correlations. J Neurol Sci. 1977 Nov;34(2):267–278. doi: 10.1016/0022-510x(77)90074-0. [DOI] [PubMed] [Google Scholar]
  12. Lynch J. C., Graybiel A. M., Lobeck L. J. The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus. J Comp Neurol. 1985 May 8;235(2):241–254. doi: 10.1002/cne.902350207. [DOI] [PubMed] [Google Scholar]
  13. Matelli M., Luppino G., Rizzolatti G. Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav Brain Res. 1985 Nov-Dec;18(2):125–136. doi: 10.1016/0166-4328(85)90068-3. [DOI] [PubMed] [Google Scholar]
  14. Mays L. E., Sparks D. L. Dissociation of visual and saccade-related responses in superior colliculus neurons. J Neurophysiol. 1980 Jan;43(1):207–232. doi: 10.1152/jn.1980.43.1.207. [DOI] [PubMed] [Google Scholar]
  15. McNaughton B. L., Barnes C. A., Gerrard J. L., Gothard K., Jung M. W., Knierim J. J., Kudrimoti H., Qin Y., Skaggs W. E., Suster M. Deciphering the hippocampal polyglot: the hippocampus as a path integration system. J Exp Biol. 1996 Jan;199(Pt 1):173–185. doi: 10.1242/jeb.199.1.173. [DOI] [PubMed] [Google Scholar]
  16. Muakkassa K. F., Strick P. L. Frontal lobe inputs to primate motor cortex: evidence for four somatotopically organized 'premotor' areas. Brain Res. 1979 Nov 9;177(1):176–182. doi: 10.1016/0006-8993(79)90928-4. [DOI] [PubMed] [Google Scholar]
  17. O'Keefe J., Conway D. H. Hippocampal place units in the freely moving rat: why they fire where they fire. Exp Brain Res. 1978 Apr 14;31(4):573–590. doi: 10.1007/BF00239813. [DOI] [PubMed] [Google Scholar]
  18. O'Keefe J., Dostrovsky J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 1971 Nov;34(1):171–175. doi: 10.1016/0006-8993(71)90358-1. [DOI] [PubMed] [Google Scholar]
  19. Ranck J. B., Jr Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. I. Behavioral correlates and firing repertoires. Exp Neurol. 1973 Nov;41(2):461–531. doi: 10.1016/0014-4886(73)90290-2. [DOI] [PubMed] [Google Scholar]
  20. Rizzolatti G., Camarda R., Fogassi L., Gentilucci M., Luppino G., Matelli M. Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res. 1988;71(3):491–507. doi: 10.1007/BF00248742. [DOI] [PubMed] [Google Scholar]
  21. Sakata H., Shibutani H., Ito Y., Tsurugai K., Mine S., Kusunoki M. Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey. Exp Brain Res. 1994;101(2):183–202. doi: 10.1007/BF00228740. [DOI] [PubMed] [Google Scholar]
  22. Sakata H., Taira M., Murata A., Mine S. Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. Cereb Cortex. 1995 Sep-Oct;5(5):429–438. doi: 10.1093/cercor/5.5.429. [DOI] [PubMed] [Google Scholar]
  23. Sharp P. E., Green C. Spatial correlates of firing patterns of single cells in the subiculum of the freely moving rat. J Neurosci. 1994 Apr;14(4):2339–2356. doi: 10.1523/JNEUROSCI.14-04-02339.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Taira M., Mine S., Georgopoulos A. P., Murata A., Sakata H. Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res. 1990;83(1):29–36. doi: 10.1007/BF00232190. [DOI] [PubMed] [Google Scholar]
  25. Touretzky D. S., Redish A. D. Theory of rodent navigation based on interacting representations of space. Hippocampus. 1996;6(3):247–270. doi: 10.1002/(SICI)1098-1063(1996)6:3<247::AID-HIPO4>3.0.CO;2-K. [DOI] [PubMed] [Google Scholar]

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

RESOURCES