Advertisement

Experimental Brain Research

, Volume 153, Issue 2, pp 158–170 | Cite as

Role of the medial parieto-occipital cortex in the control of reaching and grasping movements

  • Claudio Galletti
  • Dieter F. Kutz
  • Michela Gamberini
  • Rossella Breveglieri
  • Patrizia Fattori
Review

Abstract

The medial parieto-occipital cortex is a central node in the dorsomedial visual stream. Recent physiological studies in the macaque monkey have demonstrated that the medial parieto-occipital cortex contains two areas, the visual area V6 and the visuomotor area V6A. Area V6 is a retinotopically organized visual area that receives form and motion information directly from V1 and is heavily connected with the other areas of the dorsal visual stream, including V6A. Area V6A is a bimodal visual/somatosensory area that elaborates visual information such as form, motion and space suitable for the control of both reaching and grasping movements. Somatosensory and skeletomotor activities in V6A affect the upper limbs and involve both the transport phase of reaching and grasping movements. Finally, V6A is strongly and reciprocally connected with the dorsal premotor cortex controlling arm movements. The picture emerging from these data is that the medial parieto-occipital cortex is well equipped to control both proximal and distal movements in the online visuomotor guidance of prehension. In agreement with this view, selective V6A lesions in monkey produce misreaching and misgrasping with the arm contralateral to the lesion in visually guided movements. These deficits are similar to those observed in optic ataxia patients and suggest that human and monkey superior parietal lobules are homologous structures, and that optic ataxia syndrome is the result of the lesion of a 'human' area V6A.

Keywords

Area V6 Area V6A Dorsal visual stream Optic ataxia Visuomotor transformation Control of prehension 

Notes

Acknowledgements

This work was supported by Grants from the Ministero dell'Università e della Ricerca Scientifica e Tecnologica, Italy.

References

  1. Arbib MA (1981) Perceptual structures and distributed motor control. In: Brooks VB (ed) Motor control (Handbook of physiology, sect 1, The nervous system), vol 2. Williams and Wilkins, Baltimore, MD, pp 1449–1480Google Scholar
  2. Arbib MA, Iberall T, Lyons D (1985) Coordinated control programs for movements of the hand. Exp Brain Res (Suppl) 10:111–129Google Scholar
  3. Balint R (1909) Seelenlahmung des "Schauens", optische Ataxia, raumliche Storung der Aufmerksamkeit. Psychiatr Neurol 25:51–81Google Scholar
  4. Battaglini PP, Muzur A, Galletti C, Skrap M, Brovelli A, Fattori P (2002) Effects of lesions to area V6A in monkeys. Exp Brain Res 144:419–422CrossRefPubMedGoogle Scholar
  5. Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund HJ (1998) Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50:1253–1259PubMedGoogle Scholar
  6. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund H (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11:3276–3286CrossRefPubMedGoogle Scholar
  7. Breveglieri R, Kutz DF, Fattori P, Gamberini M, Galletti C (2002) Somatosensory cells in the parieto-occipital area V6A of the macaque. Neuroreport 13:2113–2116PubMedGoogle Scholar
  8. Bridgeman B, Lewis S, Heit G, Nagle M (1979) Relation between cognitive and motor-oriented systems of visual position perception. J Exp Psychol Hum Percept Perform 5:692–700PubMedGoogle Scholar
  9. Brodmann K (1909) Vergleichende Localisationslehre der Grosshirnrinde in Ihren Prinzipien Dargestellt auf Grund des Zellenbaues. JA Barth, LeipzigGoogle Scholar
  10. Buxbaum LJ, Coslett HB (1997) Subtypes of optic ataxia: reframing the disconnection account. Neurocase 3:159–166CrossRefGoogle Scholar
  11. Caminiti R, Johnson PB, Galli C, Ferraina S, Burnod Y (1991) Making arm movements within different parts of space: the premotor and motor cortical representation of a coordinate system for reaching to visual targets. J Neurosci 11:1182–1197PubMedGoogle Scholar
  12. Colby CL, Duhamel JR (1991) Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey. Neuropsychologia 29:517–537PubMedGoogle Scholar
  13. Colby CL, Gattass R, Olson CR, Gross CG (1988) Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study. J Comp Neurol 269:392–413PubMedGoogle Scholar
  14. Colby CL, Duhamel JR, Goldberg ME (1993) Ventral intraparietal area of the macaque: anatomic location and visual response properties. J Neurophysiol 69:902–914PubMedGoogle Scholar
  15. Desimone R, Ungerleider LG (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J Comp Neurol 248:164PubMedGoogle Scholar
  16. Desmurget M, Prablanc C (1997) Postural control of three-dimensional prehension movements. J Neurophysiol 77:452–464PubMedGoogle Scholar
  17. Desmurget M, Prablanc C, Rossetti Y, Arzi M, Paulignan Y, Urquizar C, Mignot JC (1995) Postural and synergic control for three-dimensional movements of reaching and grasping. J Neurophysiol 74:905–910PubMedGoogle Scholar
  18. Desmurget M, Prablanc C, Arzi M, Rossetti Y, Paulignan Y, Urquizar C (1996) Integrated control of hand transport and orientation during prehension movements. Exp Brain Res 110:265–278PubMedGoogle Scholar
  19. Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE, Grafton ST (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2:563–567PubMedGoogle Scholar
  20. Duhamel JR, Colby CL, Goldberg ME (1998) Ventral intraparietal area of the macaque: congruent visual and somatic response properties. J Neurophysiol 79:126–136PubMedGoogle Scholar
  21. Fattori P, Gamberini M, Kutz DF, Galletti C (1999) Spatial tuning of arm-reaching related neurons in cortical area V6A of macaque monkey. Abstr Soc Neurosci 25:152.117Google Scholar
  22. Fattori P, Gamberini M, Kutz DF, Galletti C (2001) 'Arm-reaching' neurons in the parietal area V6A of the macaque monkey. Eur J Neurosci 13:2309–2313PubMedGoogle Scholar
  23. Faugier-Grimaud S, Frenois C, Stein DG (1978) Effects of posterior parietal lesions on visually guided behavior in monkeys. Neuropsychologia 16:151–168PubMedGoogle Scholar
  24. Flanders M, Tillery SIH, Soechting JF (1992) Early stages in a sensorimotor transformation. Behav Brain Sci 15:309–362Google Scholar
  25. Fogassi L, Raos V, Franchi G, Gallese V, Luppino G, Matelli M (1999) Visual responses in the dorsal premotor area F2 of the macaque monkey. Exp Brain Res 128:194–199CrossRefPubMedGoogle Scholar
  26. Gallese V, Fadiga L, Fogassi L, Luppino G, Murata A (1997) A parietal-frontal circuit for hand grasping movements in the monkey: evidence from reversible inactivation experiments. In: Thier P, Karnath H-O (eds) Parietal lobe contributions to orientation in 3D space. Springer, Berlin Heidelberg New York, pp 255–270Google Scholar
  27. Galletti C, Battaglini PP, Fattori P (1991) Functional properties of neurons in the anterior bank of the parieto-occipital sulcus of the macaque monkey. Eur J Neurosci 3:452–461PubMedGoogle Scholar
  28. Galletti C, Battaglini PP, Fattori P (1993) Parietal neurons encoding spatial locations in craniotopic coordinates. Exp Brain Res 96:221–229PubMedGoogle Scholar
  29. Galletti C, Battaglini PP, Fattori P (1995) Eye position influence on the parieto-occipital area PO (V6) of the macaque monkey. Eur J Neurosci 7:2486–2501PubMedGoogle Scholar
  30. Galletti C, Fattori P, Battaglini PP, Shipp S, Zeki S (1996) Functional demarcation of a border between areas V6 and V6A in the superior parietal gyrus of the macaque monkey. Eur J Neurosci 8:30–52PubMedGoogle Scholar
  31. Galletti C, Fattori P, Kutz DF, Battaglini PP (1997a) Arm movement-related neurons in the visual area V6A of the macaque superior parietal lobule. Eur J Neurosci 9:410–413PubMedGoogle Scholar
  32. Galletti C, Battaglini PP, Fattori P (1997b) The posterior parietal cortex in humans and monkeys. News Physiol Sci 12:166–171Google Scholar
  33. Galletti C, Fattori P, Gamberini M, Kutz DF (1999a) The cortical visual area V6: brain location and visual topography. Eur J Neurosci 11:3922–3936CrossRefPubMedGoogle Scholar
  34. Galletti C, Fattori P, Kutz DF, Gamberini M (1999b) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582PubMedGoogle Scholar
  35. Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M (2001) The cortical connections of area V6: an occipito-parietal network processing visual information. Eur J Neurosci 13:1572–1588CrossRefPubMedGoogle Scholar
  36. Galletti C, Fattori P (2002) Posterior parietal networks encoding visual space. In: Karnath H-O, Milner AD, Vallar G (eds) The cognitive and neural bases of spatial neglect. Oxford University Press, Oxford, New York, pp 59–69Google Scholar
  37. Galletti C, Fattori P, Gamberini M, Kutz DF (2003) The most direct visual pathway to the frontal cortex. Cortex (in press)Google Scholar
  38. Gardner EP, Ro JY, Debowy D, Ghosh S (1999) Facilitation of neuronal activity in somatosensory and posterior parietal cortex during prehension. Exp Brain Res 127:329–354PubMedGoogle Scholar
  39. Gattass R, Gross CG (1981) Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. J Neurophysiol 46:621–638PubMedGoogle Scholar
  40. Gattass R, Gross CG, Sandell JH (1981) Visual topography of V2 in the macaque. J Comp Neurol 201:519–539Google Scholar
  41. Gattass R, Sousa APB, Gross CG (1988) Visuotopic organization and extent of V3 and V4 of the macaque. J Neurosci 8:1831–1845PubMedGoogle Scholar
  42. Gentilucci M, Fogassi L, Luppino G, Matelli M, Camarda R, Rizzolatti G (1988) Functional organization of inferior area 6 in the macaque monkey. I. Somatotopy and the control of proximal movements. Exp Brain Res 71:475–490PubMedGoogle Scholar
  43. Goodale MA, Pelisson D, Prablanc C (1986) Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement. Nature 320:748–750PubMedGoogle Scholar
  44. Grafton ST, Fagg AH, Woods RP, Arbib MA (1996) Functional anatomy of pointing and grasping in humans. Cereb Cortex 6:226–237PubMedGoogle Scholar
  45. Gréa H, Pisella L, Rossetti Y, Prablanc C, Desmurget M, Tilikete C, Grafton S, Vighetto A (2002) A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements. Neuropsychologia 40:2471–2480Google Scholar
  46. Haaxma R, Kuypers HG (1975) Intrahemispheric cortical connexions and visual guidance of hand and finger movements in the rhesus monkey. Brain 98:239–260PubMedGoogle Scholar
  47. Hubel DH, Wiesel TL (1977) Functional architecture of macaque monkey visual cortex. Proc R Soc Lond B Biol Sci 198:1–59PubMedGoogle Scholar
  48. Jakobson LS, Archibald YM, Carey DP, Goodale MA (1991) A kinematic analysis of reaching and grasping movements in a patient recovering from optic ataxia. Neuropsychologia 29:803–809CrossRefPubMedGoogle Scholar
  49. Jeannerod M (1981) Intersegmental coordination during reaching at natural visual objects. In: Long J, Baddeley A (eds) Attention and performance. Erlbaum, Hillsdale, pp 153–168Google Scholar
  50. Jeannerod M (1986) The formation of finger grip during prehension. A cortically mediated visuomotor pattern. Behav Brain Res 19:99–116PubMedGoogle Scholar
  51. Jeannerod M, Biguer B (1982) Visuomotor mechanisms in reaching within extrapersonal space. In: Ingle D, Goodale MA, Mansfield R (eds) Advances in the analysis of visual behavior. MIT Press, Boston, pp 387–409Google Scholar
  52. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320PubMedGoogle Scholar
  53. Kakei S, Hoffman DS, Strick PL (2001) Direction of action is represented in the ventral premotor cortex. Nat Neurosci 4:1020–1025PubMedGoogle Scholar
  54. Lewis JW, Van Essen DC (2000) Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol 428:112–137CrossRefPubMedGoogle Scholar
  55. Luppino G, Murata A, Govoni P, Matelli M (1999) Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4). Exp Brain Res 128:181–187PubMedGoogle Scholar
  56. Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J Comp Neurol 311:445–462PubMedGoogle Scholar
  57. Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G (1998) Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402:327–352PubMedGoogle Scholar
  58. Milner AD, Dijkerman HC (1998) Visual processing in the primate parietal lobe. In: Milner AD (ed) Comparative neuropsychology. Oxford University Press, Oxford, pp 70–94Google Scholar
  59. Milner AD, Goodale MA (1995) The visual brain in action. Oxford University Press, OxfordGoogle Scholar
  60. Mon-Williams M, McIntosh RD (2000) A test between two hypotheses and a possible third way for the control of prehension. Exp Brain Res 134:268–273PubMedGoogle Scholar
  61. Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210PubMedGoogle Scholar
  62. Paulignan Y, MacKenzie C, Marteniuk R, Jeannerod M (1991) Selective perturbation of visual input during prehension movements. 1. The effects of changing object position. Exp Brain Res 83:502–512PubMedGoogle Scholar
  63. Pelisson D, Prablanc C, Goodale MA, Jeannerod M (1986) Visual control of reaching movements without vision of the limb. II. Evidence of fast unconscious processes correcting the trajectory of the hand to the final position of a double-step stimulus. Exp Brain Res 62:303–311PubMedGoogle Scholar
  64. Perenin MT, Vighetto A (1988) Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111:643–674PubMedGoogle Scholar
  65. Pisella L, Grea H, Tilikete C, Vighetto A, Desmurget M, Rode G, Boisson D, Rossetti Y (2000) An 'automatic pilot' for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia. Nat Neurosci 3:729–736PubMedGoogle Scholar
  66. Prablanc C, Martin O (1992) Automatic control during hand reaching at undetected two-dimensional target displacements. J Neurophysiol 67:455–469PubMedGoogle Scholar
  67. Ratcliff G, Davies-Jones GAB (1972) Defective visual localization in focal brain wounds. Brain 95:49–60PubMedGoogle Scholar
  68. Rizzolatti G, Camarda R, Fogassi L, Gentilucci M, Luppino G, Matelli M (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distant movements. Exp Brain Res 71:491–507PubMedGoogle Scholar
  69. Rizzolatti G, Fogassi L, Gallese V (1997) Parietal cortex: from sight to action. Curr Opin Neurobiol 7:562–567PubMedGoogle Scholar
  70. Ro JY, Debowy D, Lu S, Ghosh S, Gardner EP (1998) Digital video: a tool for correlating neuronal firing patterns with hand motor behavior. J Neurosci Methods 82:215–231PubMedGoogle Scholar
  71. Rossetti Y, Pisella L, Pélisson D (2000) Eye blindness and hand sight: temporal aspects of visuomotor processing. Visual Cognit 7:785–808CrossRefGoogle Scholar
  72. Roy AC, Paulignan Y, Meunier M, Boussaoud D (2002) Prehension movements in the macaque monkey: effects of object size and location. J Neurophysiol 88:1491–1499PubMedGoogle Scholar
  73. Rushworth MFS, Nixon PD, Passingham RE (1997) Parietal cortex and movement. I. Movement selection and reaching. Exp Brain Res 117:292–310PubMedGoogle Scholar
  74. Sakata H, Taira M (1994) Parietal control of hand action. Curr Opin Neurobiol 4:847–856PubMedGoogle Scholar
  75. Shipp S, Blanton M, Zeki S (1998) A visuo-somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A. Eur J Neurosci 10:3171–3193CrossRefPubMedGoogle Scholar
  76. Smeets JB, Brenner E (1999) A new view on grasping. Motor Control 3:237–271PubMedGoogle Scholar
  77. Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386:167–170PubMedGoogle Scholar
  78. Soechting JF, Tillery SIH, Flanders M (1990) Transformation from head- to shoulder centered representation of target direction in arm movements. J Cogn Neurosci 2:32–43Google Scholar
  79. Stein J (1978) Effects of parietal lobe cooling on manipulative behaviour in the conscious monkey. In: Gordon G (ed) Active touch. Pergamon, Oxford, pp 79–90Google Scholar
  80. Stelmach GE, Castiello U, Jeannerod M (1994) Orienting the finger opposition space during prehension movements. J Mot Behav 26:178–186Google Scholar
  81. Tanné J, Boussaoud D, Boyer-Zeller N, Rouiller EM (1995) Direct visual pathways for reaching movements in the macaque monkey. Neuroreport 7:267–272PubMedGoogle Scholar
  82. Tanne-Gariepy J, Rouiller EM, Boussaoud D (2002) Parietal inputs to dorsal versus ventral premotor areas in the macaque monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91–103CrossRefPubMedGoogle Scholar
  83. Ungerleider L, Mishkin M (1982) Two cortical visual system. In: Ingle DJ, Goodale MA, Mansfield RWJ (eds) Analysis of motor behavior. MIT Press, Cambridge, MA, pp 549–586Google Scholar
  84. Wise SP, Weinrich M, Mauritz KH (1986) Movement-related activity in the premotor cortex of rhesus macaques. Prog Brain Res 64:117–131PubMedGoogle Scholar
  85. Wise SP, Boussaoud D, Johnson PB, Caminiti R (1997) Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. Annu Rev Neurosci 20:25–42PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • Claudio Galletti
    • 1
  • Dieter F. Kutz
    • 1
  • Michela Gamberini
    • 1
  • Rossella Breveglieri
    • 1
  • Patrizia Fattori
    • 1
  1. 1.Dipartimento di Fisiologia Umana e GeneraleUniversità di Bologna40127 BolognaItaly

Personalised recommendations