The Neural Control of Object-Oriented Actions

  • M. Jeannerod
Part of the NATO ASI Series book series (ASID, volume 85)


A large part of human actions are directed toward objects. Fundamental aspects of our behavior, like the ability to use tools, for example, originate from neural specialization for perceiving, grasping, recognizing and categorizing objects. These operations correspond to adaptive acquisitions in primates and some are unique to man. In this chapter, an ensemble of mechanisms for behaving with objects will be described, with emphasis on the anatomical and physiological arguments that allow to delineate a specific neural system devoted to object-oriented movements.


Superior Colliculus Mirror Neuron Posterior Parietal Cortex Grip Aperture Experimental Brain Research 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Andersen, R.A., Essik, G.K., and Siegel, R.M. (1985) Encoding of spatial location by posterior parietal neurons. Science 230, 456–458.PubMedCrossRefGoogle Scholar
  2. Arbib, M.A. (1985) Schemas for the temporal organization of behavior. Human Neurobiology 4, 63–72.PubMedGoogle Scholar
  3. Arbib, M.A. (1981) Perceptual structures and distributed motor control, in V.B. Brooks (ed.), Handbook of Physiology, Section I: The nervous system, Vol.2: Motor control,Williams et Wilkins, Baltimore, pp. 1449–1480Google Scholar
  4. Arbib, M.A and Hesse, M.B. The construction of reality. Cambridge University press, Cambridge.Google Scholar
  5. Baleydier, C. and Morel, A. (1992) Segregated thalamo-cortical pathways to infeior parietal and inferotemporal cortex in macaque monkey. Visual Neuroscience 8, 391–405.PubMedCrossRefGoogle Scholar
  6. Boussaoud, D. (1995) Primate premotor cortex. Modulation of preparatory neural activity by gaze angle. Journal of Neurophysiology 73, 886–890.PubMedGoogle Scholar
  7. Bullier, J., Girard, P., and Salin, P.A. (1994) The role of area 17 in the transfer of information to extrastriate visual cortex. Cerebral cortex 10, 301–330.Google Scholar
  8. Buys, E.J., Lemon, R.N., Mantel, G.W.H., and Muir, R.B. (1986) Selective facilitation of different hand muscles by single corticospinal neurons in the conscious monkey. Journal of Physiology 381, 529–549.PubMedGoogle Scholar
  9. Cajal, S.R. (1909) Histologie du système nerveux de l’homme et des vertébrés, Maloine, Paris.Google Scholar
  10. Caminiti, R., Johnson, P.B., and Urbano, A. (1990) Making arm movements within different parts of space: dynamic aspects in the primate motor cortex. The Journal of Neuroscience 10, 2039–2058.PubMedGoogle Scholar
  11. Caminiti, R., Johnson, P.B., Burnod, Y., Galli, C., and Ferraina, S. (1990) Shift of preferred directions of premotor cortical cells with arm movements performed across the workspace. Experimental Brain Research 83, 228–232.CrossRefGoogle Scholar
  12. Casagrande, V.A., Harting, J.K., Hall, W.C., Diamond, I.T., and Martin, G.F. (1972) Superior colliculus of the Tree Shrew: a structural and functional subdivision into superficial and deep layers. Science 177, 444–447.PubMedCrossRefGoogle Scholar
  13. Chen, D.F., Hyland, B., Maier, V, Palmeri, A., and Wiesendanger, M. (1991) Comparison of neural activity in the supplementary motoor area and in the primary motor cortex in the monkey. Somatosensory and Motor Research 8, 27–44.PubMedCrossRefGoogle Scholar
  14. Crammond, D.J. and Kalaska, J.F. (1990) Cortical neuronal activity recorded in a delay task that dissociates location of cue stimulus and movement end-point. Society for Neuroscience Abstracts 16, 423.Google Scholar
  15. Dineen, J.J. and Hendrickson, A.E. (1981) Age-correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. Investigative Ophthalmology 00000 Visual Science 21, 749–752.Google Scholar
  16. Di Pellegrino, G., Fadiga, L., Fogassi, L., Gallese, V., and Rizzolatti, G. (1992) Understanding motor events: A neurophysiological study. Experimental Brain Research 91, 176–180.CrossRefGoogle Scholar
  17. Faugier-Grimaud, S., Frenois, C., and Stein, D.G. (1978) Effects of posterior parietal lesions on visually guided behavior in monkeys. Neuropsychologia 16, 151–168.PubMedCrossRefGoogle Scholar
  18. Faugier-Grimaud, S., Frenois, C., and Peronnet, F. (1985) Effects of posterior parietal lesions on visually guided movements in monkeys. Experimental Brain Research 59, 125–138.CrossRefGoogle Scholar
  19. Fogassi, L., Gallese, V., di Pellegrino, G., Fadiga, L., Gentilucci, M., Luppino, G., Matelli, M., Pedotti, A., and Rizzolatti, G. (1992) Space coding by premotor cortex. Experimental Brain Research 89, 686–690.CrossRefGoogle Scholar
  20. Gallese, V., Murata, A., Kaseda, M., Niki, N., and Sokoto, H. (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5, 1525–1529.PubMedCrossRefGoogle Scholar
  21. Galletti, C., Battaglini, P.P., and Fattori, P. (1993) Parietal neurons encoding spatial locations in craniotopic coordinates. Experimental Brain Research 96, 221–229.CrossRefGoogle Scholar
  22. Gentilucci, M., Fogassi, L., Luppino, G., Matelli, M., Camarda, R., and Rizzolatti, G. (1988) Functional organization of inferior area 6 in the macaque monkey. 1. Somatotopy and the control of proximal movements. Experimental Brain Research 71, 475–490.CrossRefGoogle Scholar
  23. Georgopoulos, A.P., Kalaska, J.F., Caminiti, R, and Massey, J.T. (1982) On the relations between the direction of two-dimensional arm movements and cell discharge in primate motor cortex. Journal of Neuroscience 2, 1527–1537.PubMedGoogle Scholar
  24. Georgopoulos, A.P., Schwartz, A.B., and Kettner, R.E. (1986) Neuronal population coding of movement direction. Science 233, 1416–1419.PubMedCrossRefGoogle Scholar
  25. Girard, P., Salin, P., and Bullier, J. (1991) Visual activity in areas V3A and V3 during reversible inactivation of area V1 in the macaque monkey. Journal of Neurophysiology 66, 1493–1503.PubMedGoogle Scholar
  26. Girard, P., Salin, P., and Bullier, J. (1992) Response selectivity in neurons in area MT of the macaque monkey during reversible inactivation of area V1. Journal of Neurophysiology 67, 1–10.Google Scholar
  27. Glendinning, D.S., Cooper, B.Y., Vierck, C.J., and Leonard CM (1992) Altered precision grasping in stumptail macaques after fasciculus cuneatus lesions. Somatosensory and Motor Research 9, 61–73.PubMedCrossRefGoogle Scholar
  28. Goodale MA (1983) Neural mechanisms of visual orientation in rodents: targets versus places, in A. Hein and M. Jeannerod (eds)Spatially oriented behavior, Springer-Verlag, New-York, pp 35–62.Google Scholar
  29. Gordon, A.M., Forssberg, H., Johansson, R.S., and Westling, G. (1991) Visual size cues in the programming of manipulative forces during precision grip. Experimental Brain Research 83, 477–482.Google Scholar
  30. Graziano, M.S.A., Yap, G.S., and Gross, C.G. (1994) Coding of visual space by premotor neurons. Science 266, 1054–1057.PubMedCrossRefGoogle Scholar
  31. Hartje, W. and Ettlinger, G. (1973) Reaching in light and dark after unilateral posterior parietal ablations in the monkey. Cortex 9, 346–354.PubMedGoogle Scholar
  32. Heffner, R. and Masterton, B. (1975) Variation in form of the pyramidal tract and its relationship to digital dexterity. Brain, Behavior and Evolutionv 12, 161–200.CrossRefGoogle Scholar
  33. Hein, A. and Held, R. (1967) Dissociation of the visual placing response into elicited and guided components. Science 158, 190–192.CrossRefGoogle Scholar
  34. Hess, W.R., Bürgi, S., and Bucher, V. (1946) Motorische function des tectal and tegmentalgebietes. Monatsschrift für psychiatriche Neurologie 112, 1–52.CrossRefGoogle Scholar
  35. Humphrey, N.K. and Weiskrantz, L. (1967) Vision in monkeys after removal of the striate cortex. Nature 215, 595–597.PubMedCrossRefGoogle Scholar
  36. Hyvarinen, J. and Poranen, A. (1974) Function of the parietal associative area 7 as revealed from cellular discharges in alert monkeys. Brain 97, 673–692.PubMedCrossRefGoogle Scholar
  37. Iberall, T. and Arbib, M.A. (1990) Schemas for the control of hand movements: an assay on cortical localization, In: M.A. Goodale (ed),Vision and action. The control of grasping., Norwood, Ablex, pp. 204–242.Google Scholar
  38. Iberall, T., Bingham, G., and Arbib, M.A. (1986) Opposition space as a structuring concept for the analysis of skilled hand movements, in H. Heuer and C. Fromm (eds), Generation and modulation of action pattern, Experimental Brain Research Series 15: 158–173.CrossRefGoogle Scholar
  39. Jeannerod, M. (1981) Intersegmental coordination during reaching at natural visual objects, in J. Long and A. Baddeey (eds), Attention and Performance IX, Erlbaum, Hillsdale, pp. 153–168.Google Scholar
  40. Jeannerod, M. (1984) The timing of natural prehension movements. Journal of Motor Behaviour 16, 235–254.Google Scholar
  41. Jeannerod, M. (1986) The formation of finger grip during prehension. a cortically mediated visuomotor pattern. Behavioural Brain Research 19, 99–116.PubMedCrossRefGoogle Scholar
  42. Jeannerod, M. (1988) The neural and behavioural organization of goal-directed movements Oxford University Press, Oxford.Google Scholar
  43. Jeannerod M. (1994) The hand and the object. The role of posterior parietal cortex in forming motor representations. Canadian Journal of Physiology and Pharmacology 72, 525–534.CrossRefGoogle Scholar
  44. Jeannerod, M. and Biguer, B. (1982). Visuomotor mechanisms in reaching within extrapersonal space, in M.A. Goodale 00000 R. Mansfield (eds.), Advances in the analysis of visual behaviorr, MIT Press, D. Ingle, Boston, pp. 387–409Google Scholar
  45. Jeannerod, M. and Prablanc, C. (1983) The visual control of reaching movements, in: J. Desmedt (ed), Motor control mechanisms in man, Raven, New-York, pp 13–29.Google Scholar
  46. Jeannerod, M. and Rossetti, Y. (1993). Visuomotor coordination as a dissociable visual function: experimental and clinical evidences, in C. Kennard (ed.), Visual Perceptual Defects. Baillière’s Clinical Neurology, Vol.2 No.2, Baillière Tindall, pp. 439–460.Google Scholar
  47. Jeannerod, M., Arbib, M.A., Rizzolatti, G., and Sakata, H. (1995) Grasping objects. The cortical mechanisms of visuomotor transformation. Trends in Neuroscience 18, 314–320.CrossRefGoogle Scholar
  48. Johansson, R.S. and Westling, G. (1988) Coordinated isometric muscle commands adequately and erroneously programmed for the weight during lifting task with precision grip. Experimental Brain Research 71, 59–71.Google Scholar
  49. Johansson, R.S. and Westling, G. (1987) Signals in tactile afferents from the fingers eliciting adaptive motor responses during precision grip. Experimental Brain Research 66, 141–154.CrossRefGoogle Scholar
  50. Johnson, P.B., Ferraina, S., and Caminiti, R. (1993) Cortical networks for visual reaching. Experimental Brain Research 97, 361–365.CrossRefGoogle Scholar
  51. Kalaska, J.F., Caminiti, R., and Georgopoulos, A.P. (1983) Cortical mechanisms related to the direction of two dimensional arm movements. Relations in parietal area 5 and comparisonwithmotor cortex. Experimental Brain Research 51, 247–260.CrossRefGoogle Scholar
  52. Kato, M. and Tanji, J. (1972) Conscious control of motor units of human finger muscles, in: G.G. Samjen (ed), Neurophysiology studied in man, Excerpta Medica, Amsterdam.Google Scholar
  53. Lamotte, R.H. and Acuna, C. (1978) Defects in accuracy of reaching after removal of posterior parietal cortex in monkeys. Brain Research 139, 309–326.PubMedCrossRefGoogle Scholar
  54. Lemon, R.N., Mantel, G.W.H., and Muir, R.B. (1986) Corticospinal facilitation of hand muscles during voluntary movements in the conscious monkey. Journal of Physiology 381, 497–527.PubMedGoogle Scholar
  55. Lynch, J.C. (1980) The functional organization of posterior parietal association cortex. Behavioral Brain Science 3, 485–498.CrossRefGoogle Scholar
  56. MacKay, W.A. (1992). Properties of reach related neuronal activity in cortical area 7a. Journal of Neurophysiology 67, 1335–1345.PubMedGoogle Scholar
  57. Marteniuk, R.G., Leavitt, J.L., MacKenzie, C.L., and Athenes, S. (1990). Functional relationships between grasp and transport components in a prehension task. Human Movement Science 9, 149–176.CrossRefGoogle Scholar
  58. Matelli, M., Camarda, R., Glickstein, M., and Rizzolatti, R. (1986) Afferent and efferent projections of the inferior area 6 in the Macaque Monkey. The Journal of Comparative Neurology 251, 281–298.PubMedCrossRefGoogle Scholar
  59. Merigan, W.H. and Maunsell, S.H.R. (1993) How parallel are the primate visual pathways? Annual Reviews of Neuroscience 16, 369–402.CrossRefGoogle Scholar
  60. Mishkin, M. and Ungerleider, L.G. (1982) Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys. Behavioural Brain Research 6, 57–77.PubMedCrossRefGoogle Scholar
  61. Mohler, C.W. and Wurtz, R.H. (1977) Role of striate cortex and superior colliculus in visual guidance of saccadic eye movements in monkeys. Journal of Neurophysiology 40, 74–94.PubMedGoogle Scholar
  62. Morel, A. and Bullier, J. (1990) Anatomical segregation of two cortical visual pathways in the macaque monkey. Visual Neuroscience 4, 555–578.PubMedCrossRefGoogle Scholar
  63. Mountcastle, V.B., Lynch, J.C., Georgopoulos, A. Sakata, H., and Acuna, C. (1975) Posterior parietal association cortex of the monkey: command functions for operations within extra-personal space. Journal of Neurophysiology 38, 871–908.Google Scholar
  64. Muir, R.B. and Lemon, R.N. (1983) Corticospinal neurons witha special role in precision grip. Brain Research 261, 312–316.PubMedCrossRefGoogle Scholar
  65. Napier, J.R. (1956). The prehensile movements of the human hand. Journal of Bone and Joint Surgery 38B, 902–913.PubMedGoogle Scholar
  66. Napier, J.R. (1961) Prehensility and opposability in the hands of primates. Symp. Zool. Soc. London 5, 115–132.Google Scholar
  67. Peele, T.L. (1944) Acute and chronic parietal lobe ablations in monkeys. Journal of Neurophysiology 7, 269–286.Google Scholar
  68. Perrett, D.I., Harris, M.H., Bevan, R., Thomas, S., Benson, P.J., Mistlin, A.J., Citty, A.J., Hietanen, J.K., and Ortega, J.E. (1989) Framework of analysis for the neural representation of animate objects and actions. Journal of Experimental Biology 146, 87–113.PubMedGoogle Scholar
  69. Phillips, C.G. (1985) Movements of the hand. Liverpool University Press, Liverpool.Google Scholar
  70. Rizzolatti, G., Camarda, R., Fogassi, L., Gentilucci, M., Luppino, G. and Matelli, M. (1988) Functional organization of area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Experimental Brain Research 71, 491–507.CrossRefGoogle Scholar
  71. Robinson, D.L., Goldberg, M.E., and Stanton, G.B. (1978) Parietal association cortex in the primate. Sensory mechanisms and behavioural modulation. Journal of Neurophysiology 41, 910–932.PubMedGoogle Scholar
  72. Sakata, H., Shibutani, H., Ito, Y., and Tsurugai, K. (1986) Parietal cortical neurons responding to rotary movement of visual stimulus in space. Experimental Brain Research 61, 658–663.CrossRefGoogle Scholar
  73. Sakata, H., Taira, M., Mine, S., and Murata, A. (1992) Hand-movement-related neurons of the posterior parietal cortex of the monkey: their role in the visual guidance of hand movements, in R. Caminiti, P. B. Johnson and Y. Burned, (Eds), Control of arm movement in space: neurophysiological and computational approaches, Heidelberg: Springer, Berlin, pp. 185–198.CrossRefGoogle Scholar
  74. Schieber, M.H. (1990) How might the motor cortex individuate movements, TINS 13, 440–445.PubMedGoogle Scholar
  75. Schneider GE (1969) Two visual systems. Science 163, 895–902.PubMedCrossRefGoogle Scholar
  76. Shinoda, Y., Yokota, J.I., and Futami, T. (1981) Divergent projections of individual corticospinal axons to motoneurons of multiple muscles inn the monkey. Neuroscience Letters 23, 7–12.PubMedCrossRefGoogle Scholar
  77. Sivak, B. and MacKenzie, C.L. (1992) The contribution of peripheral vision and central vision to prehension, In L. Proteau and D. Elliott (Eds)Vision and motor control,Elsevier, Amsterdam.Google Scholar
  78. Sprague, J.M. and Meikie, T.H. (1965) The role of the superior colliculus in visually guided behavior. Experimental Neurology 11, 115–146.PubMedCrossRefGoogle Scholar
  79. Stelmach, G.E., Castiello, U., and Jeannerod, M. (1994) Orienting the finger opposition space during prehension movements. Journal of Motor Behavior 26, 178–186.PubMedCrossRefGoogle Scholar
  80. Taira, M., Mine, S., Georgopoulos, A.P., Murata, A., and Sakata, H. (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movements. Experimental Brain Research 83, 29–36.CrossRefGoogle Scholar
  81. Ungerleider, L. and Mishkin, M. (1982) Two cortical visual systems, in: D.J. Ingle, M.A. Goodale and R.J.W. Mansfield (Eds),Analysis of visual behavior, MIT Press, Cambridge, pp. 549–586.Google Scholar
  82. Vital-Durand, F. and Jeannerod, M. (1974) Role of visual experience in the development of optokinetic responses in kittens. Experimental Brain Research 20, 297–302.CrossRefGoogle Scholar
  83. Vital-Durand, F., Putkonen, P.T.S., and Jeannerod M. (1974) Motion detection and optokinetic responses in dark reared kittens.Vision Research 14, 141–142.Google Scholar
  84. Wallace, S.A. and Weeks, D.L. (1988). Temporal constraints in the control of prehensive movements. Journal of Motor Behavior 20, 81–105.PubMedGoogle Scholar
  85. Wannier, T.M.J., Maier, M.A., and Hepp-Reymond, M.C. (1991) Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. Journal of Neurophysiology 65, 572–589.PubMedGoogle Scholar
  86. Weiskrantz, L. (1986) Blindsight. A case study and implications, Oxford University Press, Oxford.Google Scholar
  87. Wessling, G. and Johansson, R.S. (1984) Factors influencing the force control during precisiongrip. Experimental Brain Research 53, 277–284.Google Scholar
  88. Wing, A.M. and Fraser, C. (1983). The contribution of the thumb to reaching movements. Quaterly Journal of Experimental Psychology 35A, 297–309.Google Scholar
  89. Wing, A.M., Turton, A., and Fraser, C. (1986). Grasp size and accuracy of approach in reaching. Journal of Motor Behavior 18, 245–260.PubMedGoogle Scholar
  90. Zeki, S. (1993) A vision of the brain. Blakwell, Oxford.Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 1996

Authors and Affiliations

  • M. Jeannerod
    • 1
  1. 1.Vision et MotricitéINSERM U94BronFrance

Personalised recommendations