Decoupled visually-guided reaching in optic ataxia: Differences in motor control between canonical and non-canonical orientations in space

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Granek, Joshua A ^a   Pisella, Laure ^b   Stemberger, John ^a   Vighetto, Alain ^b,c   Rossetti, Yves ^b,c,d   Sergio, Lauren E ^a  

^a YORK UNIVERSITY   (Canada)

^b LYON NEUROSCIENCE RESEARCH CENTER   (France)

^c UNIVERSITÉ DE LYON   (France)

^d HÔPITAL NEUROLOGIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ATAXIA; ENDPOINT DETERMINATION; EYE MOVEMENTS; FEMALE; HAND; HUMANS; MALE; ORIENTATION; PSYCHOMOTOR PERFORMANCE; SPACE PERCEPTION; TIME FACTORS; VISUAL PERCEPTION;

EID: 84893677636     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086138     Document Type: Article

References (90)

1. Frey SH (2007) What puts the how in where? tool use and the divided visual streams hypothesis. Cortex 43: 368-375. doi:10.1016/S0010-9452(08)70462- 3. PubMed: 17533760.
2. Gielen CC, van den Heuvel PJ, van Gisbergen JA (1984) Coordination of fast eye and arm movements in a tracking task. Exp Brain Res 56: 154-161. PubMed: 6468564.
3. Gorbet DJ, Sergio LE (2009) The behavioural consequences of dissociating the spatial directions of eye and arm movements. Brain Res 1284: 77-88. doi:10.1016/j.brainres.2009.05.057. PubMed: 19497310.
4. Neggers SF, Bekkering H (2000) Ocular gaze is anchored to the target of an ongoing pointing movement. J Neurophysiol 83: 639-651. PubMed: 10669480.
5. Neggers SF, Bekkering H (2001) Gaze anchoring to a pointing target is present during the entire pointing movement and is driven by a non-visual signal. J Neurophysiol 86: 961-970. PubMed: 11495964.
6. Sergio LE, Gorbet DJ, Tippett WJ, Yan X, Neagu B (2009) Cortical mechanisms of vision for complex action. In: M JenkinsL Harris. Cortical mechanisms of vision. Cambridge: Cambridge University Press.
7. Bock O (2005) Components of sensorimotor adaptation in young and elderly subjects. Exp Brain Res 160: 259-263. doi:10.1007/s00221-004-2133-5. PubMed: 15565436.
8. Redding GM, Rossetti Y, Wallace B (2005) Applications of prism adaptation: A tutorial in theory and method. Neurosci Biobehav Rev 29: 431-444. doi:10.1016/j.neubiorev.2004.12.004. PubMed: 15820548.
9. Redding GM, Wallace B (1996) Adaptive spatial alignment and strategic perceptual-motor control. J Exp Psychol Hum Percept Perform 22: 379-394. doi:10.1037/0096-1523.22.2.379. PubMed: 8934851.
10. Wise SP, di Pellegrino G, Boussaoud D (1996) The premotor cortex and nonstandard sensorimotor mapping. Can J Physiol Pharmacol 74: 469-482. doi:10.1139/cjpp-74-4-469. PubMed: 8828893.
11. Granek JA, Pisella L, Blangero A, Rossetti Y, Sergio LE (2012) The role of the caudal superior parietal lobule in updating hand location in peripheral vision: Further evidence from optic ataxia. PLOS ONE 7: e46619. doi:10.1371/journal.pone.0046619. PubMed: 23071599.
12. Bedford FL (1993) Perceptual and cognitive spatial learning. J Exp Psychol Hum Percept Perform 19: 517-530. PubMed: 8331313.
13. Clower DM, Boussaoud D (2000) Selective use of perceptual recalibration versus visuomotor skill acquisition. J Neurophysiol 84: 2703-2708. PubMed: 11068013.
14. Lackner JR, Dizio P (1994) Rapid adaptation to coriolis force perturbations of arm trajectory. J Neurophysiol 72: 299-313. PubMed: 7965013.
15. Jiménez L, Vaquero JM, Lupiáñez J (2006) Qualitative differences between implicit and explicit sequence learning. J Exp Psychol Learn Mem Cogn 32: 475-490. doi:10.1037/0278-7393.32.3.475. PubMed: 16719660.
16. Biguer B, Prablanc C, Jeannerod M (1984) The contribution of coordinated eye and head movements in hand pointing accuracy. Exp Brain Res 55: 462-469. PubMed: 6468552.
17. Pelz J, Hayhoe M, Loeber R (2001) The coordination of eye, head, and hand movements in a natural task. Exp Brain Res 139: 266-277. doi: 10.1007/s002210100745. PubMed: 11545465.
18. Werner S, Bock O (2010) Mechanisms for visuomotor adaptation to left-right reversed vision. Hum Mov Sci 29: 172-178. doi:10.1016/j.humov.2010. 02.004. PubMed: 20304517.
19. Connolly JD, Goodale MA, Desouza JF, Menon RS, Vilis T (2000) A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. J Neurophysiol 84: 1645-1655. PubMed: 10980034.
20. Inoue K, Kawashima R, Satoh K, Kinomura S, Sugiura M et al. (2000) A PET study of visuomotor learning under optical rotation. NeuroImage 11: 505-516. doi:10.1016/S1053-8119(00)91436-8. PubMed: 10806036.
21. Gorbet DJ, Staines WR, Sergio LE (2004) Brain mechanisms for preparing increasingly complex sensory to motor transformations. NeuroImage 23(3): 1100-1111. doi:10.1016/j.neuroimage.2004.07.043. PubMed: 15528110.
22. Granek JA, Gorbet DJ, Sergio LE (2010) Extensive video-game experience alters cortical networks for complex visuomotor transformations. Cortex 46: 1165-1177. doi:10.1016/j.cortex.2009.10.009. PubMed: 20060111.
23. Toni I, Passingham RE (1999) Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: A PET study. Exp Brain Res 127: 19-32. doi:10.1007/s002210050770. PubMed: 10424411.
24. Blangero A, Menz MM, McNamara A, Binkofski F (2009) Parietal modules for reaching. Neuropsychologia 47: 1500-1507. doi:10.1016/j.neuropsychologia.2008. 11.030. PubMed: 19109986.
25. Blangero A, Gaveau V, Luauté J, Rode G, Salemme R et al. (2008) A hand and a field effect in on-line motor control in unilateral optic ataxia. Cortex 44: 560-568. doi:10.1016/j.cortex.2007.09.004. PubMed: 18387588.
26. Khan AZ, Crawford JD, Blohm G, Urquizar C, Rossetti Y et al. (2007) Influence of initial hand and target position on reach errors in optic ataxic and normal subjects. J Vis 7: 8: 1-16. doi:10.1167/7.5.8. PubMed: 18217848.
27. Khan AZ, Pisella L, Vighetto A, Cotton F, Luauté J et al. (2005) Optic ataxia errors depend on remapped, not viewed, target location. Nat Neurosci 8: 418-420. PubMed: 15768034.
28. Pellijeff A, Bonilha L, Morgan PS, McKenzie K, Jackson SR (2006) Parietal updating of limb posture: An event-related fMRI study. Neuropsychologia 44: 2685-2690. doi:10.1016/j.neuropsychologia.2006.01.009. PubMed: 16504223.
29. Pisella L, Gréa H, Tilikete C, Vighetto A, Desmurget M et al. (2000) An 'automatic pilot' for the hand in human posterior parietal cortex: Toward reinterpreting optic ataxia. Nat Neurosci 3: 729-736. doi: 10.1038/76694. PubMed: 10862707.
30. Gréa H, Pisella L, Rossetti Y, Desmurget M, Tilikete C et al. (2002) A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements. Neuropsychologia 40: 2471-2480. doi: 10.1016/S0028-3932(02)00009-X. PubMed: 12417474.
31. 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 (3): 643-674. doi:10.1093/brain/111.3.643.
32. Prado J, Clavagnier S, Otzenberger H, Scheiber C, Kennedy H et al. (2005) Two cortical systems for reaching in central and peripheral vision. Neuron 48: 849-858. doi:10.1016/j.neuron.2005.10.010. PubMed: 16337921.
33. Blangero A, Ota H, Delporte L, Revol P, Vindras P, et al. (2007) Optic ataxia is not only 'optic': Impaired spatial integration of proprioceptive information. Neuroimage 36 Suppl 2: T61-8
34. Pisella L, Sergio L, Blangero A, Torchin H, Vighetto A et al. (2009) Optic ataxia and the function of the dorsal stream: Contributions to perception and action. Neuropsychologia 47: 3033-3044. doi:10.1016/j.neuropsychologia.2009. 06.020. PubMed: 19563817.
35. Pisella L, Binkofski F, Lasek K, Toni I, Rossetti Y (2006) No double-dissociation between optic ataxia and visual agnosia: Multiple substreams for multiple visuo-manual integrations. Neuropsychologia 44: 2734-2748. doi:10.1016/j.neuropsychologia.2006.03.027. PubMed: 16753188.
36. Rossetti Y, Pisella L, Vighetto A (2003) Optic ataxia revisited: Visually guided action versus immediate visuomotor control. Exp Brain Res 153: 171-179. doi:10.1007/s00221-003-1590-6. PubMed: 13680044.
37. Buiatti T, Skrap M, Shallice T (2013) Reaching a moveable visual target: Dissociations in brain tumour patients. Brain Cogn 82: 6-17. doi: 10.1016/j.bandc.2013.02.004. PubMed: 23501699.
38. Krakauer JW, Pine ZM, Ghilardi MF, Ghez C (2000) Learning of visuomotor transformations for vectorial planning of reaching trajectories. J Neurosci 20: 8916-8924. PubMed: 11102502.
39. Werner S, Bock O (2007) Effects of variable practice and declarative knowledge on sensorimotor adaptation to rotated visual feedback. Exp Brain Res 178: 554-559. doi:10.1007/s00221-007-0925-0. PubMed: 17361424.
40. Mazzoni P, Krakauer JW (2006) An implicit plan overrides an explicit strategy during visuomotor adaptation. J Neurosci 26: 3642-3645. doi: 10.1523/JNEUROSCI.5317-05.2006. PubMed: 16597717.
41. Benson BL, Anguera JA, Seidler RD (2011) A spatial explicit strategy reduces error but interferes with sensorimotor adaptation. J Neurophysiol 105: 2843-2851. doi:10.1152/jn.00002.2011. PubMed: 21451054.
42. Cunningham HA (1989) Aiming error under transformed spatial mappings suggests a structure for visual-motor maps. J Exp Psychol Hum Percept Perform 15: 493-506. doi:10.1037/0096-1523.15.3.493. PubMed: 2527958.
43. Abeele S, Bock O (2001) Sensorimotor adaptation to rotated visual input: Different mechanisms for small versus large rotations. Exp Brain Res 140: 407-410. doi:10.1007/s002210100846. PubMed: 11685393.
44. Bock O, Abeele S, Eversheim U (2003) Human adaptation to rotated vision: Interplay of a continuous and a discrete process. Exp Brain Res 152: 528-532. doi:10.1007/s00221-003-1643-x. PubMed: 14513189.
45. Bock O (2013) Basic principles of sensorimotor adaptation to different distortions with different effectors and movement types: A review and synthesis of behavioral findings. Front Hum Neuroscience 7: 81. PubMed: 23503204.
46. Jeannerod M, Decety J, Michel F (1994) Impairment of grasping movements following a bilateral posterior parietal lesion. Neuropsychologia 32: 369-380. doi:10.1016/0028-3932(94)90084-1 PubMed: 8047246.
47. Battaglia-Mayer A, Ferrari-Toniolo S, Visco-Comandini F, Archambault PS, Saberi-Moghadam S et al. (2012) Impairment of online control of hand and eye movements in a monkey model of optic ataxia. Cereb Cortex.
48. Oldfield RC (1971) The assessment and analysis of handedness: The edinburgh inventory. Neuropsychologia 9: 97-113. doi: 10.1016/0028-3932(71) 90067-4. PubMed: 5146491.
49. Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain: 3-dimensional proportional system - an approach to cerebral imaging. New York, NY: Thieme Medical Publishers.
50. Karnath HO, Perenin MT (2005) Cortical control of visually guided reaching: Evidence from patients with optic ataxia. Cereb Cortex 15: 1561-1569. doi:10.1093/cercor/bhi034. PubMed: 15716470.
51. Rossetti Y, Revol P, McIntosh R, Pisella L, Rode G et al. (2005) Visually guided reaching: Bilateral posterior parietal lesions cause a switch from fast visuomotor to slow cognitive control. Neuropsychologia 43: 162-177. doi:10.1016/j.neuropsychologia.2004.11.004. PubMed: 15707902.
52. Newport R, Brown L, Husain M, Mort D, Jackson SR (2006) The role of the posterior parietal lobe in prism adaptation: Failure to adapt to optical prisms in a patient with bilateral damage to posterior parietal cortex. Cortex 42: 720-729. doi:10.1016/S0010-9452(08)70410-6. PubMed: 16909632.
53. Crawford JR, Garthwaite PH, Porter S (2010) Point and interval estimates of effect sizes for the case-controls design in neuropsychology: Rationale, methods, implementations, and proposed reporting standards. Cogn Neuropsychol 27: 245-260. doi: 10.1080/02643294.2010.513967. PubMed: 20936548.
54. Vesia M, Yan X, Henriques DY, Sergio LE, Crawford JD (2008) Transcranial magnetic stimulation over human dorsal-lateral posterior parietal cortex disrupts integration of hand position signals into the reach plan. J Neurophysiol 100: 2005-2014. doi:10.1152/jn.90519.2008. PubMed: 18684904.
55. Novak KE, Miller LE, Houk JC (2002) The use of overlapping submovements in the control of rapid hand movements. Exp Brain Res 144: 351-364. doi:10.1007/s00221-002-1060-6. PubMed: 12021817.
56. Milner AD, Goodale MA, editors (1995) The visual brain in action.
57. Brogaard B (2011) Conscious vision for action versus unconscious vision for action? Cogn Sci 35: 1076-1104. doi:10.1111/j.1551-6709.2011.01171.x. PubMed: 21790744.
58. Schenk T, McIntosh RD (2010) Do we have independent visual streams for perception and action? Journal of Cognitive Neuroscience 1: 52-63. doi:10.1080/17588920903388950. PubMed: 24168245.
59. Pisella L, André V, Gavault E, Le Flem A, Luc-Pupat E et al. (2013) A test revealing the slow acquisition and the dorsal stream substrate of visuo-spatial perception. Neuropsychologia 51: 106-113. doi:10.1016/j. neuropsychologia.2012.11.015. PubMed: 23174400.
60. Clavagnier S, Prado J, Kennedy H, Perenin MT (2007) How humans reach: Distinct cortical systems for central and peripheral vision. Neuroscientist 13: 22-27. doi:10.1177/1073858406295688. PubMed: 17229972.
61. Hawkins KM, Sayegh P, Yan X, Crawford JD, Sergio LE (2013) Neural activity in superior parietal cortex during rule-based visual-motor transformations. J Cogn Neurosci 25: 436-454. doi:10.1162/jocn-a-00318. PubMed: 23092356.
62. Revol P, Rossetti Y, Vighetto A, Rode G, Boisson D et al. (2003) Pointing errors in immediate and delayed conditions in unilateral optic ataxia. Spat Vis 16: 347-364. doi:10.1163/156856803322467572. PubMed: 12858956.
63. Trillenberg P, Sprenger A, Petersen D, Kompf D, Heide W, et al. (2007) Functional dissociation of saccade and hand reaching control with bilateral lesions of the medial wall of the intraparietal sulcus: Implications for optic ataxia. Neuroimage 36 Suppl 2: T69-76
64. Milner AD, Dijkerman HC, McIntosh RD, Rossetti Y, Pisella L (2003) Delayed reaching and grasping in patients with optic ataxia. Prog Brain Res 142: 225-242. doi:10.1016/S0079-6123(03)42016-5. PubMed: 12693264.
65. Thaler L, Goodale MA (2011) Reaction times for allocentric movements are 35 ms slower than reaction times for target-directed movements. Exp Brain Res 211: 313-328. doi:10.1007/s00221-011-2691-2. PubMed: 21516448.
66. James TW, Culham J, Humphrey GK, Milner AD, Goodale MA (2003) Ventral occipital lesions impair object recognition but not object-directed grasping: An fMRI study. Brain 126: 2463-2475. doi:10.1093/brain/awg248. PubMed: 14506065.
67. Schenk T (2006) An allocentric rather than perceptual deficit in patient d.f. Nat Neurosci 9: 1369-1370. doi:10.1038/nn1784. PubMed: 17028584.
68. Milner AD, Goodale MA, editors (2006) The visual brain in action (2nd edition).
69. Maunsell JH, van Essen DC (1983) The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci 3: 2563-2586. PubMed: 6655500.
70. Rozzi S, Calzavara R, Belmalih A, Borra E, Gregoriou GG et al. (2006) Cortical connections of the inferior parietal cortical convexity of the macaque monkey. Cereb Cortex 16: 1389-1417. PubMed: 16306322.
71. Buxbaum LJ (2007) Complex object-related actions: Structure, meaning, and context. J Int Neuropsychol Soc 13: 993-996. PubMed: 17942017.
72. Husain M, Nachev P (2007) Space and the parietal cortex. Trends Cogn Sci 11: 30-36. doi:10.1016/j.tics.2006.10.011. PubMed: 17134935.
73. Blangero A, Ota H, Rossetti Y, Fujii T, Ohtake H et al. (2010) Systematic retinotopic reaching error vectors in unilateral optic ataxia. Cortex 46: 77-93. doi:10.1016/j.cortex.2009.02.015. PubMed: 19345345.
74. Battaglini PP, Muzur A, Galletti C, Skrap M, Brovelli A et al. (2002) Effects of lesions to area V6A in monkeys. Exp Brain Res 144: 419-422. doi:10.1007/s00221-002-1099-4. PubMed: 12021823.
75. Gail A, Andersen RA (2006) Neural dynamics in monkey parietal reach region reflect context-specific sensorimotor transformations. J Neurosci 26: 9376-9384. doi:10.1523/JNEUROSCI.1570-06.2006. PubMed: 16971521.
76. Batista AP, Andersen RA (2001) The parietal reach region codes the next planned movement in a sequential reach task. J Neurophysiol 85: 539-544. PubMed: 11160491.
77. Snyder LH, Batista AP, Andersen RA (1997) Coding of intention in the posterior parietal cortex. Nature 386: 167-170. doi:10.1038/386167a0. PubMed: 9062187.
78. Andersen RA, Brotchie PR, Mazzoni P (1992) Evidence for the lateral intraparietal area as the parietal eye field. Curr Opin Neurobiol 2: 840-846. doi:10.1016/0959-4388(92)90143-9. PubMed: 1477549.
79. Cui H, Andersen RA (2007) Posterior parietal cortex encodes autonomously selected motor plans. Neuron 56: 552-559. doi:10.1016/j.neuron.2007.09.031. PubMed: 17988637.
80. Jackson SR, Newport R, Mort D, Husain M (2005) Where the eye looks, the hand follows; limb-dependent magnetic misreaching in optic ataxia. Curr Biol 15: 42-46. doi:10.1016/j.cub.2004.12.049. PubMed: 15649363.
81. Jackson SR, Newport R, Husain M, Fowlie JE, O'Donoghue M et al. (2009) There may be more to reaching than meets the eye: Re-thinking optic ataxia. Neuropsychologia 47: 1397-1408. doi:10.1016/j.neuropsychologia.2009.01.035. PubMed: 19428405.
82. Battaglia-Mayer A, Caminiti R (2002) Optic ataxia as a result of the breakdown of the global tuning fields of parietal neurones. Brain 125: 225-237. doi:10.1093/brain/awf034. PubMed: 11844724.
83. Battaglia-Mayer A, Ferraina S, Mitsuda T, Marconi B, Genovesio A et al. (2000) Early coding of reaching in the parietooccipital cortex. J Neurophysiol 83: 2374-2391. PubMed: 10758140.
84. Sayegh PF, Hawkins KM, Hoffman KL, Sergio LE (2013) Differences in spectral profiles between rostral and caudal premotor cortex when eye-hand actions are decoupled. J Neurophysiol.
85. Flanagan JR, Bowman MC, Johansson RS (2006) Control strategies in object manipulation tasks. Curr Opin Neurobiol 16: 650-659. doi: 10.1016/j.conb.2006. 10.005. PubMed: 17084619.
86. Prablanc C, Echallier JF, Komilis E, Jeannerod M (1979) Optimal response of eye and hand motor systems in pointing at a visual target. I. spatio-temporal characteristics of eye and hand movements and their relationships when varying the amount of visual information. Biol Cybern 35: 113-124. doi:10.1007/ BF00337436. PubMed: 518932.
87. Desmurget M, Epstein CM, Turner RS, Prablanc C, Alexander GE et al. (1999) Role of the posterior parietal cortex in updating reaching movements to a visual target. Nat Neurosci 2: 563-567. doi: 10.1038/9219. PubMed: 10448222.
88. Himmelbach M, Nau M, Zündorf I, Erb M, Perenin MT et al. (2009) Brain activation during immediate and delayed reaching in optic ataxia. Neuropsychologia 47: 1508-1517. doi:10.1016/j.neuropsychologia.2009.01.033. PubMed: 19428407.
89. Fernandez-Ruiz J, Goltz HC, DeSouza JFX, Vilis T, Crawford JD (2007) Human parietal "reach region" primarily encodes intrinsic visual direction, not extrinsic movement direction, in a visual-motor dissociation task. Cerebral Cortex 17: 2283-2292. doi:10.1093/cercor/bhl137. PubMed: 17215478.
90. Vesia M, Prime SL, Yan X, Sergio LE, Crawford JD (2010) Specificity of human parietal saccade and reach regions during transcranial magnetic stimulation. J Neurosci 30: 13053-13065. doi:10.1523/JNEUROSCI.1644-10.2010. PubMed: 20881123.