Functional magnetic resonance adaptation reveals the involvement of the dorsomedial stream in hand orientation for grasping

Journal of Neurophysiology

Volumn 106, Issue 5, 2011, Pages 2248-2263

  Monaco, Simona ^a   Cavina Pratesi, Cristiana ^b   Sedda, Anna ^c   Fattori, Patrizia ^d   Galletti, Claudio ^d   Culhaml, Jody C ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b DURHAM UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF PAVIA   (Italy)

^d UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Anterior intraparietal sulcus; Reaching; Superior parieto occipital cortex; V6A; Wrist

Indexed keywords

ADULT; ARTICLE; BODY POSTURE; BRAIN; CONTROLLED STUDY; FEMALE; FINGER; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GRIP STRENGTH; HAND; HUMAN; INTRAPARIETAL SULCUS; LEFT HEMISPHERE; MALE; OCCIPITAL CORTEX; ORIENTATION; PRIORITY JOURNAL; RIGHT HANDEDNESS; RIGHT HEMISPHERE; THUMB; TOUCH; VISUAL FEEDBACK; WRIST;

ADULT; ARM; BIOMECHANICS; FEMALE; FUNCTIONAL LATERALITY; HAND; HAND STRENGTH; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OCCIPITAL LOBE; ORIENTATION; PARIETAL LOBE; PSYCHOMOTOR PERFORMANCE; WRIST JOINT;

EID: 80755130181     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01069.2010     Document Type: Article

References (103)

1. Arbib MA. Perceptual structures and distributed motor control. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am Physiol Soc, 1981, sect. 2, vol. II, part 1, p. 1449-1480.
2. Battaglini PP, Muzur A, Galletti C, Skrap M, Brovelli A, Fattori P. Effects of lesions to area V6A in monkeys. Exp Brain Res 144: 419-422, 2002.
3. Baumann MA, Fluet MC, Scherberger H. Context-specific grasp movement representation in the macaque anterior intraparietal area. J Neurosci 29: 6436-6448, 2009.
4. Begliomini C, Caria A, Grodd W, Castiello U. Comparing natural and constrained movements: new insights into the visuomotor control of grasping. PLoS One 2: e1108, 2007a.
5. Begliomini C, Wall MB, Smith AT, Castiello U. Differential cortical activity for precision and whole-hand visually guided grasping in humans. Eur J Neurosci 25: 1245-1252, 2007b.
6. Belia S, Fidler F, Williams J, Cumming G. Researchers misunderstand confidence intervals and standard error bars. Psychol Methods 10: 389-396, 2005.
7. Binkofski F, Dohle C, Posse S, Stephan KM, Hefter H, Seitz RJ, Freund HJ. Human anterior intraparietal area subserves prehension: a combined lesion and functional MRI activation study. Neurology 50: 1253-1259, 1998.
8. Boynton GM, Finney EM. Orientation-specific adaptation in human visual cortex. J Neurosci 23: 8781-8787, 2003.
9. Breveglieri R, Kutz DF, Fattori P, Gamberini M, Galletti C. Somatosensory cells in the parieto occipital area V6A of the macaque. Neuroreport 13: 2113-2116, 2002.
10. Bristow D, Frith C, Rees G. Two distinct neural effects of blinking on human visual processing. Neuroimage 27: 136-145, 2005.
11. Caminiti R, Genovesio A, Marconi B, Mayer AB, Onorati P, Ferraina S, Mitsuda T, Giannetti S, Squatrito S, Maioli MG, Molinari M. Early coding of reaching: frontal and parietal association connections of parietooccipital cortex. Eur J Neurosci 11: 3339-3345, 1999.
12. Castiello U, Begliomini C. The cortical control of visually guided grasping. Neuroscientist 14: 157-170, 2008.
13. Cavina-Pratesi C, Goodale MA, Culham JC. FMRI reveals a dissociation between grasping and perceiving the size of real 3D objects. PLoS One 2: e424, 2007.
14. Cavina-Pratesi C, Ietswaart M, Humphreys GW, Lestou V, Milner AD. Impaired grasping in a patient with optic ataxia: primary visuomotor deficit or secondary consequence of misreaching? Neuropsychologia 48: 226-234, 2010a.
15. Cavina-Pratesi C, Monaco S, Fattori P, Galletti C, McAdam TD, Quinlan DJ, Goodale MA, Culham JC. Functional magnetic resonance imaging reveals the neural substrates of arm transport and grip formation in reachto- grasp actions in humans. J Neurosci 30: 10306-10323, 2010b.
16. Chouinard PA, Paus T. The primary motor and premotor areas of the human cerebral cortex. Neuroscientist 12: 143-152, 2006.
17. Culham JC, Danckert SL, DeSouza JF, Gati JS, Menon RS, Goodale MA. Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas. Exp Brain Res 153: 180-189, 2003.
18. De Baene W, Vogels R. Effects of adaptation on the stimulus selectivity of macaque inferior temporal spiking activity and local field potentials. Cereb Cortex 20: 2145-2165, 2010.
19. de Jong BM, van der Graaf FH, Paans AM. Brain activation related to the representations of external space and body scheme in visuomotor control. Neuroimage 14: 1128-1135, 2001.
20. Desmurget M, Prablanc C, Arzi M, Rossetti Y, Paulignan Y, Urquizar C. Integrated control of hand transport and orientation during prehension movements. Exp Brain Res 110: 265-278, 1996.
21. Faillenot I, Decety J, Jeannerod M. Human brain activity related to the perception of spatial features of objects. Neuroimage 10: 114-124, 1999.
22. Faillenot I, Toni I, Decety J, Gregoire MC, Jeannerod M. Visual pathways for object-oriented action and object recognition: functional anatomy with PET. Cereb Cortex 7: 77-85, 1997.
23. Fan J, He J, Tillery SI. Control of hand orientation and arm movement during reach and grasp. Exp Brain Res 171: 283-296, 2006.
24. Fattori P, Breveglieri R, Amoroso K, Galletti C. Evidence for both reaching and grasping activity in the medial parieto-occipital cortex of the macaque. Eur J Neurosci 20: 2457-2466, 2004.
25. Fattori P, Breveglieri R, Marzocchi N, Filippini D, Bosco A, Galletti C. Hand orientation during reach-to-grasp movements modulates neuronal activity in the medial posterior parietal area V6A. J Neurosci 29: 1928-1936, 2009.
26. Fattori P, Gamberini M, Kutz DF, Galletti C. ''Arm-reaching'' neurons in the parietal area V6A of the macaque monkey. Eur J Neurosci 13: 2309-2313, 2001.
27. Fattori P, Raos V, Breveglieri R, Bosco A, Marzocchi N, Galletti C. The dorsomedial pathway is not just for reaching: grasping neurons in the medial parieto-occipital cortex of the macaque monkey. J Neurosci 30: 342-349, 2010.
28. Faugier-Grimaud S, Frenois C, Peronnet F. Effects of posterior parietal lesions on visually guided movements in monkeys. Exp Brain Res 59: 125-138, 1985.
29. Faugier-Grimaud S, Frenois C, Stein DG. Effects of posterior parietal lesions on visually guided behavior in monkeys. Neuropsychologia 16: 151-168, 1978.
30. Filimon F. Human cortical control of hand movements: parietofrontal networks for reaching, grasping, and pointing. Neuroscientist 16: 388-407, 2010.
31. Frey SH, Vinton D, Norlund R, Grafton ST. Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Brain Res Cogn Brain Res 23: 397-405, 2005.
32. Galletti C, Fattori P, Gamberini M, Kutz DF. The cortical visual area V6: brain location and visual topography. Eur J Neurosci 11: 3922-3936, 1999.
33. Galletti C, Gamberini M, Kutz DF, Fattori P, Luppino G, Matelli M. The cortical connections of area V6: an occipito-parietal network processing visual information. Eur J Neurosci 13: 1572-1588, 2001.
34. Galletti C, Kutz DF, Gamberini M, Breveglieri R, Fattori P. Role of the medial parieto-occipital cortex in the control of reaching and grasping movements. Exp Brain Res 153: 158-170, 2003.
35. Gallivan JP, Cavina-Pratesi C, Culham JC. Is that within reach? fMRI reveals that the human superior parieto-occipital cortex encodes objects reachable by the hand. J Neurosci 29: 4381-4391, 2009.
36. Gamberini M, Passarelli L, Fattori P, Zucchelli M, Bakola S, Luppino G, Galletti C. Cortical connections of the visuomotor parietooccipital area V6Ad of the macaque monkey. J Comp Neurol 513: 622-642, 2009.
37. Gamberini M, Galletti C, Bosco A, Breveglieri R, Fattori P. Is the medial posterior parietal area V6A a single functional area? J Neurosci 31: 5145-5157, 2011.
38. Grill-Spector K, Henson R, Martin A. Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn Sci 10: 14-23, 2006.
39. Grol MJ, Majdandzic J, Stephan KE, Verhagen L, Dijkerman HC, Bekkering H, Verstraten FA, Toni I. Parieto-frontal connectivity during visually guided grasping. J Neurosci 27: 11877-11887, 2007.
40. Hazelton FT, Smidt GL, Flatt AE, Stephens RI. The influence of wrist position on the force produced by the finger flexors. J Biomech 8: 301-306, 1975.
41. Herbort O, Butz MV. Planning and control of hand orientation in grasping movements. Exp Brain Res 202: 867-878, 2010.
42. Hesse C, Deubel H. Changes in grasping kinematics due to different start postures of the hand. Hum Mov Sci 28: 415-436, 2009.
43. Jacobs S, Danielmeier C, Frey SH. Human anterior intraparietal and ventral premotor cortices support representations of grasping with the hand or a novel tool. J Cogn Neurosci 22: 2594-2608, 2010.
44. Jakobson LS, Archibald YM, Carey DP, Goodale MA. A kinematic analysis of reaching and grasping movements in a patient recovering from optic ataxia. Neuropsychologia 29: 803-809, 1991.
45. James TW, Humphrey GK, Gati JS, Menon RS, Goodale MA. Differential effects of viewpoint on object-driven activation in dorsal and ventral streams. Neuron 35: 793-801, 2002.
46. Jeannerod M. The hand and the object: the role of posterior parietal cortex in forming motor representations. Can J Physiol Pharmacol 72: 535-541, 1994.
47. Jeannerod M. Mechanisms of visuomotor coordination: a study in normal and brain damaged subjects. Neuropsychologia 24: 41-78, 1986.
48. Jeannerod M. Specialized channels for cognitive responses. Cognition 10: 135-137, 1981.
49. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18: 314-320, 1995.
50. Johnson SH. Thinking ahead: the case for motor imagery in prospective judgements of prehension. Cognition 74: 33-70, 2000.
51. Johnson SH, Rotte M, Grafton ST, Hinrichs H, Gazzaniga MS, Heinze HJ. Selective activation of a parietofrontal circuit during implicitly imagined prehension. Neuroimage 17: 1693-1704, 2002.
52. Johnston JA, Bobich LR, Santello M. Coordination of intrinsic and extrinsic hand muscle activity as a function of wrist joint angle during two-digit grasping. Neurosci Lett 474: 104-108, 2010.
53. Kamitani Y, Tong F. Decoding the visual and subjective contents of the human brain. Nat Neurosci 8: 679-685, 2005.
54. Karnath HO, Perenin MT. Cortical control of visually guided reaching: evidence from patients with optic ataxia. Cereb Cortex 15: 1561-1569, 2005.
55. Katsuyama N, Yamashita A, Sawada K, Naganuma T, Sakata H, Taira M. Functional and histological properties of caudal intraparietal area of macaque monkey. Neuroscience 167: 1-10, 2010.
56. Kroliczak G, Cavina-Pratesi C, Goodman DA, Culham JC. What does the brain do when you fake it? An FMRI study of pantomimed and real grasping. J Neurophysiol 97: 2410-2422, 2007.
57. Kroliczak G, McAdam TD, Quinlan DJ, Culham JC. The human dorsal stream adapts to real actions and 3D shape processing: a functional magnetic resonance imaging study. J Neurophysiol 100: 2627-2639, 2008.
58. Lacquaniti F, Soechting JF. Coordination of arm and wrist motion during a reaching task. J Neurosci 2: 399-408, 1982.
59. Larsson J, Landy MS, Heeger DJ. Orientation-selective adaptation to firstand second-order patterns in human visual cortex. J Neurophysiol 95: 862-881, 2006.
60. Lieberman MD, Cunningham WA. Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 4: 423-428, 2009.
61. Linscheid RL. Kinematic considerations of the wrist. Clin Orthop Relat Res 202: 27-39, 1986.
62. Loftus GR, Masson MEJ. Using confidence intervals in within-subject designs. Psychon Bull Rev 1: 476-490, 1994.
63. Luppino G, Hamed SB, Gamberini M, Matelli M, Galletti C. Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto-occipital sulcus of the macaque: a cytoarchitectonic study. Eur J Neurosci 21: 3056-3076, 2005.
64. Marangon M, Jacobs S, Frey SH. Evidence for context sensitivity of grasp representations in human parietal and premotor cortices. J Neurophysiol 105: 2536-2546, 2011.
65. Matelli M, Govoni P, Galletti C, Kutz DF, Luppino G. Superior area 6 afferents from the superior parietal lobule in the macaque monkey. J Comp Neurol 402: 327-352, 1998.
66. Monaco S, Sedda A, Cavina-Pratesi C, Culham CJ. Where is it? How big is it? Different brain areas answer different questions about graspable three-dimensional object properties in an fMRI adaptation experiment. Soc Neurosci Abstr 2010: 893.3, 2010.
67. Mur M, Ruff DA, Bodurka J, Bandettini PA, Kriegeskorte N. Face-identity change activation outside the face system: ''release from adaptation'' may not always indicate neuronal selectivity. Cereb Cortex 20: 2027-2042, 2010.
68. Murata A, Gallese V, Luppino G, Kaseda M, Sakata H. Selectivity for the shape, size, and orientation of objects for grasping in neurons of monkey parietal area AIP. J Neurophysiol 83: 2580-2601, 2000.
69. Ogawa S, Tank DW, Menon R, Ellermann JM, Kim SG, Merkle H, Ugurbil K. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 89: 5951-5955, 1992.
70. Palastanga N, Field D, Soames R. Anatomy and Human Movement: Structure and Function. Oxford, UK: Butterworth Heinemann, 1989, p. 672.
71. Passarelli L, Rosa MG, Gamberini M, Bakola S, Burman KJ, Fattori P, Galletti C. Cortical connections of area V6Av in the macaque: a visualinput node to the eye/hand coordination system. J Neurosci 31: 1790-1801, 2011.
72. Perenin MT, Vighetto A. Optic ataxia: a specific disruption in visuomotor mechanisms. I. Different aspects of the deficit in reaching for objects. Brain 111: 643-674, 1988.
73. Pitzalis S, Galletti C, Huang RS, Patria F, Committeri G, Galati G, Fattori P, Sereno MI. Wide-field retinotopy defines human cortical visual area v6. J Neurosci 26: 7962-7973, 2006.
74. Pitzalis S, Sereno MI, Committeri G, Fattori P, Galati G, Patria F, Galletti C. Human v6: the medial motion area. Cereb Cortex 20: 411-424, 2010.
75. Portin K, Salenius S, Salmelin R, Hari R. Activation of the human occipital and parietal cortex by pattern and luminance stimuli: neuromagnetic measurements. Cereb Cortex 8: 253-260, 1998.
76. Prado J, Clavagnier S, Otzenberger H, Scheiber C, Kennedy H, Perenin MT. Two cortical systems for reaching in central and peripheral vision. Neuron 48: 849-858, 2005.
77. Quinlan DJ, Culham JC. fMRI reveals a preference for near viewing in the human parieto-occipital cortex. Neuroimage 36: 167-187, 2007.
78. Raos V, Umilta MA, Gallese V, Fogassi L. Functional properties of graspingrelated neurons in the dorsal premotor area F2 of the macaque monkey. J Neurophysiol 92: 1990-2002, 2004.
79. Rice NJ, Valyear KF, Goodale MA, Milner AD, Culham JC. Orientation sensitivity to graspable objects: an fMRI adaptation study. Neuroimage 36, Suppl 2: T87-T93, 2007.
80. Rizzolatti G, Luppino G, Matelli M. The organization of the cortical motor system: new concepts. Electroencephalogr Clin Neurophysiol 106: 283-296, 1998.
81. Rosenbaum DA, Vaughan J, Barnes HJ, Jorgensen MJ. Time course of movement planning: selection of handgrips for object manipulation. J Exp Psychol Learn Mem Cogn 18: 1058-1073, 1992.
82. Sakata H, Taira M, Kusunoki M, Murata A, Tanaka Y, Tsutsui K. Neural coding of 3D features of objects for hand action in the parietal cortex of the monkey. Philos Trans R Soc Lond B Biol Sci 353: 1363-1373, 1998.
83. Sapountzis P, Schluppeck D, Bowtell R, Peirce JW. A comparison of fMRI adaptation and multivariate pattern classification analysis in visual cortex. Neuroimage 49: 1632-1640, 2010.
84. Sawamura H, Orban GA, Vogels R. Selectivity of neuronal adaptation does not match response selectivity: a single-cell study of the FMRI adaptation paradigm. Neuron 49: 307-318, 2006.
85. Saxe R, Brett M, Kanwisher N. Divide and conquer: a defense of functional localizers. Neuroimage 30: 1088-1096, 2006.
86. Scannell JW, Young MP. Neuronal population activity and functional imaging. Proc Biol Sci 266: 875-881, 1999.
87. Shallice T, Venable N, Rumiati RI. Dissociable distal and proximal motor components: evidence from perseverative errors in three apraxic patients. Cogn Neuropsychol 22: 625-639, 2005.
88. Shikata E, Hamzei F, Glauche V, Knab R, Dettmers C, Weiller C, Buchel C. Surface orientation discrimination activates caudal and anterior intraparietal sulcus in humans: an event-related fMRI study. J Neurophysiol 85: 1309-1314, 2001.
89. Shikata E, Hamzei F, Glauche V, Koch M, Weiller C, Binkofski F, Buchel C. Functional properties and interaction of the anterior and posterior intraparietal areas in humans. Eur J Neurosci 17: 1105-1110, 2003.
90. Shipp S, Blanton M, Zeki S. A visuo-somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A. Eur J Neurosci 10: 3171-3193, 1998.
91. Stelmach GE, Castiello U, Jeannerod M. Orienting the finger opposition space during prehension movements. J Mot Behav 26: 178-186, 1994.
92. Summerfield C, Trittschuh EH, Monti JM, Mesulam MM, Egner T. Neural repetition suppression reflects fulfilled perceptual expectations. Nat Neurosci 11: 1004-1006, 2008.
93. Taira M, Mine S, Georgopoulos AP, Murata A, Sakata H. Parietal cortex neurons of the monkey related to the visual guidance of hand movement. Exp Brain Res 83: 29-36, 1990.
94. Talairach J, Tournoux P. Co-planar Stereotaxic Atlas of the Human Brain. New York: Thieme Medical, 1988.
95. Tam F, Matenine D, Bachmutsky V, Graham JS. Video-based monitoring for fMRI of uncontrolled movements. Proc Int Soc Magn Reson Med 17th Sci Mtg 2009: Abstract 1197, 2009.
96. Taubert M, Dafotakis M, Sparing R, Eickhoff S, Leuchte S, Fink GR, Nowak DA. Inhibition of the anterior intraparietal area and the dorsal premotor cortex interfere with arbitrary visuo-motor mapping. Clin Neurophysiol 121: 408-413, 2010.
97. Tsutsui K, Jiang M, Sakata H, Taira M. Short-term memory and perceptual decision for three-dimensional visual features in the caudal intraparietal sulcus (area CIP). J Neurosci 23: 5486-5495, 2003.
98. Tsutsui K, Jiang M, Yara K, Sakata H, Taira M. Integration of perspective and disparity cues in surface-orientation-selective neurons of area CIP. J Neurophysiol 86: 2856-2867, 2001.
99. Tsutsui K, Sakata H, Naganuma T, Taira M. Neural correlates for perception of 3D surface orientation from texture gradient. Science 298: 409-412, 2002.
100. Tunik E, Frey SH, Grafton ST. Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp. Nat Neurosci 8: 505-511, 2005.
101. Valyear KF, Culham JC, Sharif N, Westwood D, Goodale MA. A double dissociation between sensitivity to changes in object identity and object orientation in the ventral and dorsal visual streams: a human fMRI study. Neuropsychologia 44: 218-228, 2006.
102. Vanni S, Tanskanen T, Seppa M, Uutela K, Hari R. Coinciding early activation of the human primary visual cortex and anteromedial cuneus. Proc Natl Acad Sci USA 98: 2776-2780, 2001.
103. Wood DK, Monaco S, McAdam T, Dutton GN, Culham CJ, Goodae MA. Impaired selection of wrist posture in a patient with a parieto-occipital lesion. Soc Neurosci Abstr 2009: 307.5, 2009.