Skip to main content
Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1998 Aug 29;353(1373):1363–1373. doi: 10.1098/rstb.1998.0290

Neural coding of 3D features of objects for hand action in the parietal cortex of the monkey.

H Sakata 1, M Taira 1, M Kusunoki 1, A Murata 1, Y Tanaka 1, K Tsutsui 1
PMCID: PMC1692338  PMID: 9770229

Abstract

In our previous studies of hand manipulation task-related neurons, we found many neurons of the parietal association cortex which responded to the sight of three-dimensional (3D) objects. Most of the task-related neurons in the AIP area (the lateral bank of the anterior intraparietal sulcus) were visually responsive and half of them responded to objects for manipulation. Most of these neurons were selective for the 3D features of the objects. More recently, we have found binocular visual neurons in the lateral bank of the caudal intraparietal sulcus (c-IPS area) that preferentially respond to a luminous bar or place at a particular orientation in space. We studied the responses of axis-orientation selective (AOS) neurons and surface-orientation selective (SOS) neurons in this area with stimuli presented on a 3D computer graphics display. The AOS neurons showed a stronger response to elongated stimuli and showed tuning to the orientation of the longitudinal axis. Many of them preferred a tilted stimulus in depth and appeared to be sensitive to orientation disparity and/or width disparity. The SOS neurons showed a stronger response to a flat than to an elongated stimulus and showed tuning to the 3D orientation of the surface. Their responses increased with the width or length of the stimulus. A considerable number of SOS neurons responded to a square in a random dot stereogram and were tuned to orientation in depth, suggesting their sensitivity to the gradient of disparity. We also found several SOS neurons that responded to a square with tilted or slanted contours, suggesting their sensitivity to orientation disparity and/or width disparity. Area c-IPS is likely to send visual signals of the 3D features of an object to area AIP for the visual guidance of hand actions.

Full Text

The Full Text of this article is available as a PDF (369.0 KB).

Selected References

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

  1. Barlow H. B., Blakemore C., Pettigrew J. D. The neural mechanism of binocular depth discrimination. J Physiol. 1967 Nov;193(2):327–342. doi: 10.1113/jphysiol.1967.sp008360. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Blakemore C., Fiorentini A., Maffei L. A second neural mechanism of binocular depth discrimination. J Physiol. 1972 Nov;226(3):725–749. doi: 10.1113/jphysiol.1972.sp010006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. De Renzi E., Faglioni P., Scotti G. Judgment of spatial orientation in patients with focal brain damage. J Neurol Neurosurg Psychiatry. 1971 Oct;34(5):489–495. doi: 10.1136/jnnp.34.5.489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dijkerman H. C., Milner A. D., Carey D. P. The perception and prehension of objects oriented in the depth plane. I. Effects of visual form agnosia. Exp Brain Res. 1996 Dec;112(3):442–451. doi: 10.1007/BF00227950. [DOI] [PubMed] [Google Scholar]
  5. ETTLINGER G., WARRINGTON E., ZANGWILL O. L. A further study of visual-spatial agnosia. Brain. 1957 Sep;80(3):335–361. doi: 10.1093/brain/80.3.335. [DOI] [PubMed] [Google Scholar]
  6. Goodale M. A., Milner A. D., Jakobson L. S., Carey D. P. A neurological dissociation between perceiving objects and grasping them. Nature. 1991 Jan 10;349(6305):154–156. doi: 10.1038/349154a0. [DOI] [PubMed] [Google Scholar]
  7. Goodale M. A., Milner A. D. Separate visual pathways for perception and action. Trends Neurosci. 1992 Jan;15(1):20–25. doi: 10.1016/0166-2236(92)90344-8. [DOI] [PubMed] [Google Scholar]
  8. HECAEN H., PENFIELD W., BERTRAND C., MALMO R. The syndrome of apractognosia due to lesions of the minor cerebral hemisphere. AMA Arch Neurol Psychiatry. 1956 Apr;75(4):400–434. [PubMed] [Google Scholar]
  9. Hubel D. H., Livingstone M. S. Segregation of form, color, and stereopsis in primate area 18. J Neurosci. 1987 Nov;7(11):3378–3415. doi: 10.1523/JNEUROSCI.07-11-03378.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Hyvärinen J., Poranen A. Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. Brain. 1974 Dec;97(4):673–692. doi: 10.1093/brain/97.1.673. [DOI] [PubMed] [Google Scholar]
  11. Jeannerod M., Decety J., Michel F. Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia. 1994 Apr;32(4):369–380. doi: 10.1016/0028-3932(94)90084-1. [DOI] [PubMed] [Google Scholar]
  12. Matelli M., Camarda R., Glickstein M., Rizzolatti G. Afferent and efferent projections of the inferior area 6 in the macaque monkey. J Comp Neurol. 1986 Sep 15;251(3):281–298. doi: 10.1002/cne.902510302. [DOI] [PubMed] [Google Scholar]
  13. McFIE J., PIERCY M. F., ZANGWILL O. L. Visual-spatial agnosia associated with lesions of the right cerebral hemisphere. Brain. 1950 Jun;73(2):167–190. doi: 10.1093/brain/73.2.167. [DOI] [PubMed] [Google Scholar]
  14. Milner A. D., Perrett D. I., Johnston R. S., Benson P. J., Jordan T. R., Heeley D. W., Bettucci D., Mortara F., Mutani R., Terazzi E. Perception and action in 'visual form agnosia'. Brain. 1991 Feb;114(Pt 1B):405–428. doi: 10.1093/brain/114.1.405. [DOI] [PubMed] [Google Scholar]
  15. Mountcastle V. B., Lynch J. C., Georgopoulos A., Sakata H., Acuna C. Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol. 1975 Jul;38(4):871–908. doi: 10.1152/jn.1975.38.4.871. [DOI] [PubMed] [Google Scholar]
  16. Murata A., Gallese V., Kaseda M., Sakata H. Parietal neurons related to memory-guided hand manipulation. J Neurophysiol. 1996 May;75(5):2180–2186. doi: 10.1152/jn.1996.75.5.2180. [DOI] [PubMed] [Google Scholar]
  17. Nikara T., Bishop P. O., Pettigrew J. D. Analysis of retinal correspondence by studying receptive fields of binocular single units in cat striate cortex. Exp Brain Res. 1968;6(4):353–372. doi: 10.1007/BF00233184. [DOI] [PubMed] [Google Scholar]
  18. PIERCY M., HECAEN H., de AJURIAGUERRA Constructional apraxia associated with unilateral cerebral lesions-left and right sided cases compared. Brain. 1960;83:225–242. doi: 10.1093/brain/83.2.225. [DOI] [PubMed] [Google Scholar]
  19. Perenin M. T., Vighetto A. Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain. 1988 Jun;111(Pt 3):643–674. doi: 10.1093/brain/111.3.643. [DOI] [PubMed] [Google Scholar]
  20. Poggio G. F., Fischer B. Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J Neurophysiol. 1977 Nov;40(6):1392–1405. doi: 10.1152/jn.1977.40.6.1392. [DOI] [PubMed] [Google Scholar]
  21. Poggio G. F., Gonzalez F., Krause F. Stereoscopic mechanisms in monkey visual cortex: binocular correlation and disparity selectivity. J Neurosci. 1988 Dec;8(12):4531–4550. doi: 10.1523/JNEUROSCI.08-12-04531.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. 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]
  23. Sakata H., Taira M., Kusunoki M., Murata A., Tanaka Y. The TINS Lecture. The parietal association cortex in depth perception and visual control of hand action. Trends Neurosci. 1997 Aug;20(8):350–357. doi: 10.1016/s0166-2236(97)01067-9. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. Sakata H., Taira M. Parietal control of hand action. Curr Opin Neurobiol. 1994 Dec;4(6):847–856. doi: 10.1016/0959-4388(94)90133-3. [DOI] [PubMed] [Google Scholar]
  26. Shikata E., Tanaka Y., Nakamura H., Taira M., Sakata H. Selectivity of the parietal visual neurones in 3D orientation of surface of stereoscopic stimuli. Neuroreport. 1996 Oct 2;7(14):2389–2394. doi: 10.1097/00001756-199610020-00022. [DOI] [PubMed] [Google Scholar]
  27. Sutherland N. S. The representation of three-dimensional objects. Nature. 1979 Mar 29;278(5703):395–398. doi: 10.1038/278395a0. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. 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]
  30. Zeki S. M. The third visual complex of rhesus monkey prestriate cortex. J Physiol. 1978 Apr;277:245–272. doi: 10.1113/jphysiol.1978.sp012271. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES