Experimental Brain Research

, Volume 153, Issue 2, pp 146–157 | Cite as

Two different streams form the dorsal visual system: anatomy and functions

Review

Abstract

There are two radically different views on the functional role of the dorsal visual stream. One considers it as a system involved in space perception. The other is of a system that codes visual information for action organization. On the basis of new anatomical data and a reconsideration of previous functional and clinical data, we propose that the dorsal stream and its recipient parietal areas form two distinct functional systems: the dorso-dorsal stream (d-d stream) and the ventro-dorsal stream (v-d stream). The d-d stream is formed by area V6 (main d-d extrastriate visual node) and areas V6A and MIP of the superior parietal lobule. Its major functional role is the control of actions "on line". Its damage leads to optic ataxia. The v-d stream is formed by area MT (main v-d extrastriate visual node) and by the visual areas of the inferior parietal lobule. As the d-d stream, v-d stream is responsible for action organization. It, however, also plays a crucial role in space perception and action understanding. The putative mechanisms linking action and perception in the v-d stream is discussed.

Keywords

Dorsal visual stream Parietal lobe Action Perception 

Notes

Acknowledgements

We are grateful to Giuseppe Luppino for his help and critical discussion of the manuscript. This study was supported by CNR (Consiglio Nazionale delle Ricerche) and by MIUR (Ministero dell'Istruzione, dell'Università e della Ricerca).

References

  1. Bell BD (1994) Pantomime recognition impairment in aphasia: an analysis of error types. Brain Lang 47:269–278CrossRefPubMedGoogle Scholar
  2. Berti A, Rizzolatti G (1992) Visual processing without awareness: Evidence from unilateral neglect. J Cognit Neurosci 4:345–351Google Scholar
  3. 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
  4. Binkofski F, Buccino G, Posse S, Seitz RJ, Rizzolatti G, Freund HJ (1999) A fronto-parietal circuit for object manipulation in man: evidence from an fMRI-study. Eur J Neurosci 11:3276–3286CrossRefPubMedGoogle Scholar
  5. Bisiach E, Vallar G (2000) Unilateral neglect in humans. In: Boller F, Grafman J, Rizzolatti G (eds) Handbook of neuropsychology, vol. I, 2nd edn. Elsevier Science, Amsterdam, pp 459–450Google Scholar
  6. Brain WR (1961) Speech disorders: aphasia, apraxia and agnosia. Butterworth, WashingtonGoogle Scholar
  7. Brodmann K (1909) Vergleichende Lokalisationslehre der Grosshirnrinde in ihren Prinzipien Dargerstellt auf Grund des Zellenbaues. Barth, LeipzigGoogle Scholar
  8. Bruce CJ, Desimone R, Gross CG (1981) Visual properties of neurons in a polisensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369–384PubMedGoogle Scholar
  9. Buccino G, Lui F, Patteri I, Benuzzi F, Canessa N, Lagravinese G, Porro CA, Rizzolatti G (2002) Observation of actions performed by non-conspecifics activates the mirror system in humans. Soc Neurosci 163.1Google Scholar
  10. Caminiti R, Ferraina S, Johnson PB (1996) The sources of visual information to the primate frontal lobe: a novel role for the superior parietal lobule. Cereb Cortex 6:319–328PubMedGoogle Scholar
  11. Chao LL, Martin A (2000) Representation of manipulable man-made objects in the dorsal stream. Neuroimage 12:478–484CrossRefPubMedGoogle Scholar
  12. Colby CL, Duhamel JR (1991) Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkeys. 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: anatomical location and visual response properties. J Neurophysiol 69:902–914PubMedGoogle Scholar
  15. Cooke DF, Taylor CSR, Moore T, Graziano MSE (2002) Electrical microstimulation in monkey area VIP evokes defensive movements. Soc Neurosci Abstr 560.1Google Scholar
  16. Cowey A, Small M, Ellis S (1994) Left visuo-spatial neglect can be worse in far than near space. Neuropsychologia 32:1059–1066PubMedGoogle Scholar
  17. D'Esposito M, McGlinchey-Berroth R, Alexander MP, Verfaellie M, Milberg WP (1993) Dissociable cognitive and neural mechanisms of unilateral visual neglect. Neurology 43:2638–2644PubMedGoogle Scholar
  18. De Renzi E (1982) Disorders of space exploration and cognition. John Wiley, Chichester, UKGoogle Scholar
  19. De Renzi E, Faglioni P (1999) Apraxia. In: Denes G, Pizzamiglio (eds) Clinical and experimental neuropsychology. Psychology Press, East Sussex, UKGoogle Scholar
  20. Desimone R, Gross CG (1979) Visual areas in the temporal cortex of the macaque monkey. Brain Res 178:363–380PubMedGoogle Scholar
  21. Duffy JR, Watkins LB (1984) The effect of response choice relatedness on pantomime and verbal recognition ability in aphasic patients. Brain Lang 21:291–306PubMedGoogle Scholar
  22. Duhamel JR, Bremmer F, Ben Hamed S, Graf W (1997) Spatial invariance of visual receptive fields in parietal cortex neurons. Nature 389:845–848PubMedGoogle Scholar
  23. Ehrsson HH, Fagergren A, Jonsson T, Westling G, Johansson RS, Forssberg H (2000) Cortical activity in precision- versus power-grip tasks: an fMRI study. J Neurophysiol 83:528–536PubMedGoogle Scholar
  24. Fogassi L, Gallese V, Fadiga L, Luppino G, Matelli M, Rizzolatti G (1996) Coding of peripersonal space in inferior premotor cortex (area F4). J Neurophysiol 76:141–157PubMedGoogle Scholar
  25. Fogassi L, Gallese V, Fadiga L, Rizzolatti G (1998) Neurons responding to the sight of goal-directed hand/arm actions in the parietal area PF (7b) of the macaque monkey. Soc Neurosci Abstr 24:257–255Google Scholar
  26. Fogassi L, Gallese V, Buccino G, Craighero L, Fadiga L, Rizzolatti G (2001) Cortical mechanism for the visual guidance of hand grasping movements in the monkey: A reversible inactivation study. Brain 124:571–586PubMedGoogle Scholar
  27. Gainotti G, Lemmo MS (1976) Comprehension of symbolic gestures in aphasia. Brain Lang 3:451–460PubMedGoogle Scholar
  28. Gallese V, Murata A, Kaseda M, Niki N, Sakata H (1994) Deficit of hand preshaping after muscimol injection in monkey parietal cortex. Neuroreport 5:1525–1529PubMedGoogle Scholar
  29. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119:593–609PubMedGoogle Scholar
  30. Gallese V, Fadiga L, Fogassi L, Rizzolatti G (2002) Action representation and the inferior parietal lobule. In: Prinz W, Hommel B (eds) Common mechanisms in perception and action: attention and performance, vol. XIX. Oxford University Press, UK, pp 334–355Google Scholar
  31. 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
  32. Galletti C, Fattori P, Kutz DF, Battaglini PP (1999) Brain location and visual topography of cortical area V6A in the macaque monkey. Eur J Neurosci 11:575–582PubMedGoogle Scholar
  33. Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M (2001) The cortical connections of area V6A: an occipito-parietal network processing visual information. Eur J Neurosci 13:1572–1588CrossRefPubMedGoogle Scholar
  34. Gamberini M, Galletti C, Luppino G, Matelli M (2002) Cytoarchitectonic organization of the functionally defined areas V6 and V6A in the parieto-occipital cortex of macaque brain. J Physiol (Lond) 543P, 113PGoogle Scholar
  35. Gentilucci M, Scandolara C, Pigarev IN, Rizzolatti G (1983) Visual responses in the postarcuate cortex (area 6) of the monkey that are independent of eye position. Exp Brain Res 50:464–468PubMedGoogle Scholar
  36. 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 7:475–490Google Scholar
  37. Gerardin E, Sirigu A, Lehericy S, Poline J-B, Gaymard B, Marsault C, Agid Y, Le Bihan D (2000) Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex 10:1093–1104CrossRefPubMedGoogle Scholar
  38. Geschwind N (1965) Disconnexion syndromes in animals and man. Brain 88:237–294PubMedGoogle Scholar
  39. Godschalk M, Lemon RN, Nijs HGT, Kuypers HGJM (1981) Behavior of neurons in monkey peri-arcuate and precentral cortex before and during visually guided arm and hand movements. Exp Brain Res 44:113–116PubMedGoogle Scholar
  40. Goodale MA, Milner AD (1992) Separate visual pathways for perception and action. Trends Neurosci 15:20–25PubMedGoogle Scholar
  41. Graziano MS, Yap GS, Gross CG (1994) Coding of visual space by premotor neurons. Science 266:1054–1057PubMedGoogle Scholar
  42. Graziano MS, Taylor CS, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851PubMedGoogle Scholar
  43. Halligan PW, Marshall JC (1991) Left neglect for near but not far space in man. Nature 350:498–500Google Scholar
  44. Heilman KM, Rothi LJ, Valenstein E (1982) Two forms of ideomotor apraxia. Neurology 32:342–346PubMedGoogle Scholar
  45. Helmoltz H (1896) Die Tatsache der Wahrnehmung. In: Vorträge und Reden, vol. II. BraunschweigGoogle Scholar
  46. Hyvärinen J (1981) Regional distribution of functions in parietal association area 7 of the monkey. Brain Res 206:287–303CrossRefPubMedGoogle Scholar
  47. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC, Rizzolatti G (1999) Cortical mechanisms of human imitation. Science 286:2526–2528PubMedGoogle Scholar
  48. Jeannerod M (1986) The formation of finger grip during prehension. A cortically mediated visuomotor pattern. Behav Brain Sci 19:99–116CrossRefGoogle Scholar
  49. Jeannerod M (1994) The representing brain: neural correlates of motor intention and imagery. Behav Brain Sci 17:187–245Google Scholar
  50. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H (1995) Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18:314–320PubMedGoogle Scholar
  51. Johnson PB, Ferraina S, Caminiti R (1993) Cortical networks for visual reaching. Exp Brain Res 97:361–365PubMedGoogle Scholar
  52. Johnson PB, Ferraina S, Bianchi L, Caminiti R (1996) Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. Cereb Cortex 6:102–119PubMedGoogle Scholar
  53. Karnath HO, Ferber S, Himmelbach M (2001) Spatial awareness is a function of the temporal not the posterior parietal lobe. Nature 411:950–953Google Scholar
  54. Lacquaniti F, Guigon E, Bianchi L, Ferraina S, Caminiti R (1995) Representing spatial information for limb movement: role of area 5 in the monkey. Cereb Cortex 5:391–409PubMedGoogle Scholar
  55. Leinonen L, Hyvärinen J, Nyman G, Linnankoski I (1979) I. Function properties of neurons in lateral part of associative area 7 in awake monkeys. Exp Brain Res 34:299–320PubMedGoogle Scholar
  56. Marshall JF, Halligan PW (1988) Blindsight and insight in visuo-spatial neglect. Nature 336:766–767CrossRefPubMedGoogle Scholar
  57. Matelli M, Luppino G, Rizzolatti G (1985) Patterns of cytochrome oxidase activity in the frontal agranular cortex of macaque monkey. Behav Brain Res 18:125–137PubMedGoogle Scholar
  58. Matelli M, Luppino G, Rizzolatti G (1991) Architecture of superior and mesial area 6 and of the adjacent cingulate cortex. J Comp Neurol 311:445–462PubMedGoogle Scholar
  59. 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
  60. Milner D, Goodale MA (1995) The visual brain in action. Oxford University Press, OxfordGoogle Scholar
  61. Mountcastle VB, Lynch JC, Georgopoulos A, Sakata H, Acuna C (1975) Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. J Neurophysiol 38:871–908PubMedGoogle Scholar
  62. Murata A, Fadiga L, Fogassi L, Gallese V, Raos V, Rizzolatti G (1997) Object representation in the ventral premotor cortex (area F5) of the monkey. J Neurophysiol 78:2226–2230Google Scholar
  63. Murata A, Gallese V, Luppino G, Kaseda M, Sakata H (2000) Selectivity for the shape, size and orientation of objects in the hand-manipulation-related neurons in the anterior intraparietal (AIP) area of the macaque. J Neurophysiol 83:2580–2601PubMedGoogle Scholar
  64. Nishitani N, Hari R (2000) Temporal dynamics of cortical representation for action. Proc Natl Acad Sci U S A 97:913–918PubMedGoogle Scholar
  65. Pandya DN, Seltzer B (1982) Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J Comp Neurol 204:196–210PubMedGoogle Scholar
  66. Pause M, Kunesch E, Binkofski F, Freund HJ (1989) Sensorimotor disturbances in patients with lesions of the parietal cortex. Brain 112:1599–1625PubMedGoogle Scholar
  67. 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
  68. Perrett DI, Harries MH, Bevan R, Thomas S, Benson PJ, Mistlin AJ, Chitty AK, Hietanen JK, Ortega JE (1989) Frameworks of analysis for the neural representation of animate objects and actions. J Exp Biol 146:87–113PubMedGoogle Scholar
  69. Petrides M, Pandya DN (1997) Comparative architectonic analysis of the human and the macaque frontal cortex. In: Boller F, Grafman J (eds) Handbook of neuropsychology, vol. IX. Elsevier, New York, pp 17–58Google Scholar
  70. Ratcliff G, Davies Jones GAB (1972) Defective visual localization in focal brain wounds. Brain 95:49–60PubMedGoogle Scholar
  71. Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901PubMedGoogle Scholar
  72. Rizzolatti G, Matelli M, Pavesi G (1983) Deficits in attention and movement following the removal of postarcuate (area 6) and prearcuate (area 8) cortex in macaque monkeys. Brain 106:655–673PubMedGoogle Scholar
  73. 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 distal movements. Exp Brain Res 71:491–507PubMedGoogle Scholar
  74. Rizzolatti G, Fadiga L, Gallese V, Fogassi L (1996) Premotor cortex and the recognition of motor actions. Cognit Brain Res 3:131–141CrossRefGoogle Scholar
  75. Rizzolatti G, Berti A, Gallese V (2000) Spatial neglect: neurophysiological bases, cortical circuits and theories. In: Boller F, Grafman J, Rizzolatti G (eds) Handbook of neuropsychology, vol. I. 2nd edn. Elsevier Science, Amsterdam, pp 503–537Google Scholar
  76. Rizzolatti G, Fogassi L, Gallese V (2001) Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Rev Neurosci 2:661–670CrossRefGoogle Scholar
  77. Rothi LJ, Heilman KM, Watson RT (1985) Pantomime comprehension and ideomotor apraxia. J Neurol Neurosurg Psychiatry 48:451–454Google Scholar
  78. Sakata H, Taira M (1994) Parietal control of hand action. Curr Opin Neurobiol 4:847–856PubMedGoogle Scholar
  79. Sakata H, Takaoka Y, Kawarasaki A, Shibutani H (1973) Somatosensory properties of neurons in the superior parietal cortex (area 5) of the rhesus monkey. Brain Res 64:85–102PubMedGoogle Scholar
  80. Schieber M (2000) Inactivation of the ventral premotor cortex biases the laterality of motoric choices. Exp Brain Res 130:497–507CrossRefPubMedGoogle Scholar
  81. 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
  82. Sperry RW (1952) Neurology and the mind-brain problem. Am Sci 40:291–312Google Scholar
  83. Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H (1990) Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res 83:29–36PubMedGoogle Scholar
  84. Tanné J, Boussaoud D, Boyerzeller N, Rouiller EM (1995) Direct visual pathways for reaching movement in the macaque monkeys. Neuroreport 7:267–272PubMedGoogle Scholar
  85. Tanné-Gariepy J, Rouiller EM, Boussaoud D (2002) Parietal inputs to dorsal versus ventral premotor areas in the monkey: evidence for largely segregated visuomotor pathways. Exp Brain Res 145:91–103CrossRefPubMedGoogle Scholar
  86. Ungerleider LG, Mishkin M (1982) Two visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT Press, Cambridge, MA, pp 549–586Google Scholar
  87. Vallar G, Perani D (1987) The anatomy of spatial neglect in humans. In: Jeannerod M (ed) Neurophysiological and neuropsychological aspects of spatial neglect. North-Holland Elsevier Science, Amsterdam, pp 235–258Google Scholar
  88. Von Bonin G, Bailey P (1947) The neocortex of Macaca mulatta. University of Illinois Press, Urbana Il, pp 136Google Scholar
  89. Von Economo C (1929) The cytoarchitectonics of the human cerebral cortex. Oxford University Press, London, pp 186Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Dipartimento di NeuroscienzeUniversità di ParmaParmaItaly

Personalised recommendations