Simultaneous encoding of the direction and orientation of potential targets during reach planning: Evidence of multiple competing reach plans

Journal of Neurophysiology

Volumn 110, Issue 4, 2013, Pages 807-816

  Stewart, Brandie M ^a   Baugh, Lee A ^b   Gallivan, Jason P ^a,c   Flanagan, J Randall ^a,c  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF SOUTH DAKOTA   (United States)

^c QUEEN S UNIVERSITY   (Canada)

Author keywords

Decision making; Goal directed action; Human; Visually guided reaching

Indexed keywords

ADULT; ARTICLE; BRAIN REGION; CLINICAL ARTICLE; DECISION MAKING; FEMALE; HAND MOVEMENT; HUMAN; MALE; ORIENTATION; PLANNING; PRIORITY JOURNAL; REACTION TIME; VISUAL FEEDBACK;

EID: 84881642963     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00131.2013     Document Type: Article

References (73)

1. Andersen RA, Buneo CA. Intentional maps in posterior parietal cortex. Annu Rev Neurosci 25: 189-220, 2002.
2. Andersen RA, Cui H. Intention, action planning, and decision making in parietal-frontal circuits. Neuron 63: 568-583, 2009.
3. Arai K, McPeek RM, Keller EL. Properties of saccadic responses in monkey when multiple competing visual stimuli are present. J Neurophysiol 91: 890-900, 2004.
4. Baldauf D, Deubel H. Attentional landscapes in reaching and grasping. Vision Res 50: 999-1013, 2010.
5. Basso MA, Wurtz RH. Modulation of neuronal activity by target uncertainty. Nature 389: 66-69, 1997.
6. Baumann MA, Fluet MC, Scherberger H. Context-specific grasp movement representation in the macaque anterior intraparietal area. J Neurosci 29: 6436-6448, 2009.
7. Beck JM, Ma WJ, Kiani R, Hanks T, Churchland AK, Roitman J, Shadlen MN, Latham PE, Pouget A. Probabilistic population codes for bayesian decision making. Neuron 60: 1142-1152, 2008.
8. Brenner E, Smeets JB. Fast responses of the human hand to changes in target position. J Mot Behav 29: 297-310, 1997.
9. Chapman CS, Gallivan JP, Wood DK, Milne JL, Culham JC, Goodale MA. Reaching for the unknown: multiple target encoding and real-time decision-making in a rapid reach task. Cognition 116: 168-176, 2010a.
10. Chapman CS, Gallivan JP, Wood DK, Milne JL, Culham JC, Goodale MA. Short-term motor plasticity revealed in a visuomotor decision-making task. Behav Brain Res 214: 130-134, 2010b.
11. Cisek P. Cortical mechanisms of action selection: the affordance competition hypothesis. Philos Trans R Soc Lond B Biol Sci 362: 1585-1599, 2007.
12. Cisek P. Integrated neural processes for defining potential actions and deciding between them: a computational model. J Neurosci 26: 9761-9770, 2006.
13. Cisek P. Making decisions through a distributed consensus. Curr Opin Neurobiol 22: 927-936, 2012.
14. Cisek P, Kalaska JF. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 45: 801-814, 2005.
15. Cisek P, Kalaska JF. Simultaneous encoding of multiple potential reach directions in dorsal premotor cortex. J Neurophysiol 87: 1149-1154, 2002.
16. 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.
17. Desmurget M, Prablanc C, Rossetti Y, Arzi M, Paulignan Y, Urquizar C, Mignot JC. Postural and synergic control for three-dimensional movements of reaching and grasping. J Neurophysiol 74: 905-910, 1995.
18. Diedrichsen J, Shadmehr R, Ivry RB. The coordination of movement: optimal feedback control and beyond. Trends Cogn Sci 14: 31-39, 2010.
19. Fan J, He J, Tillery SI. Control of hand orientation and arm movement during reach and grasp. Exp Brain Res 171: 283-296, 2006.
20. 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.
21. 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.
22. Findlay JM, Walker R. A model of saccade generation based on parallel processing and competitive inhibition. Behav Brain Sci 22: 661-721, 1999.
23. Gallivan JP, Chapman CS, Wood DK, Milne JL, Ansari D, Culham JC, Goodale MA. One to four, and nothing more: nonconscious parallel dividuation of objects during action planning. Psychol Sci 22: 803-811, 2011a.
24. Gallivan JP, McLean DA, Flanagan JR, Culham JC. Where one hand meets the other: limb-specific and action-dependent movement plans decoded from preparatory signals in single human frontoparietal brain areas. J Neurosci 33: 1991-2008, 2013.
25. Gallivan JP, McLean DA, Smith FW, Culham JC. Decoding effectordependent and effector-independent movement intentions from human parieto-frontal brain activity. J Neurosci 31: 17149-17168, 2011b.
26. Ghez C, Favilla M, Ghilardi MF, Gordon J, Bermejo R, Pullman S. Discrete and continuous planning of hand movements and isometric force trajectories. Exp Brain Res 115: 217-233, 1997.
27. Glimcher PW, Sparks DL. Representation of averaging saccades in the superior colliculus of the monkey. Exp Brain Res 95: 429-435, 1993.
28. Godijn R, Theeuwes J. Programming of endogenous and exogenous saccades: evidence for a competitive integration model. J Exp Psychol Hum Percept Perform 28: 1039-1054, 2002.
29. Gomi H. Implicit online corrections of reaching movements. Curr Opin Neurobiol 18: 558-564, 2008.
30. Grafton ST. The cognitive neuroscience of prehension: recent developments. Exp Brain Res 204: 475-491, 2010.
31. Grol MJ, Majdandzic J, Stephan KE, Verhagen L, Dijkerman C, Bekkering H, Verstraten F, Toni I. Parieto-frontal connectivity during visually guided grasping. J Neurosci 27: 11877-11887, 2007.
32. Hanley JR, Young AW, Pearson NA. Impairment of the visuo-spatial sketch pad. Q J Exp Psychol A 43: 101-125, 1991.
33. Hyun JS, Luck SJ. Visual working memory as the substrate for mental rotation. Psychon Bull Rev 14: 154-158, 2007.
34. Jeannerod M. Intersegmental coordination during reaching at natural visual objects. In: Attention and Performance IX, edited by Long J and Baddeley A. New York: Lawrence Erlbaum Associates, 1981, p. 153-168.
35. Jeannerod M. The Neural and Behavioural Organization of Goal-Directed Movements. Oxford, UK: Oxford Univ. Press Psychology Series no. 5, 1988.
36. Jeannerod M. The timing of natural prehension movements. J Mot Behav 16: 235-254, 1984.
37. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends Neurosci 18: 314-320, 1995.
38. Johnson SH, Grafton ST. From 'acting on' to 'acting with': the functional anatomy of object-oriented action schemata. Prog Brain Res 142: 127-139, 2003.
39. Luck SJ, Vogel EK. The capacity of visual working memory for features and conjunctions. Nature 390: 279-281, 1997.
40. MacEvoy SP, Epstein RA. Constructing scenes from objects in human occipitotemporal cortex. Nat Neurosci 14: 1323-1329, 2011.
41. MacEvoy SP, Epstein RA. Decoding the representation of multiple simultaneous objects in human occipitotemporal cortex. Curr Biol 19: 943-947, 2009.
42. MacEvoy SP, Tucker TR, Fitzpatrick D. A precise form of divisive suppression supports population coding in the primary visual cortex. Nat Neurosci 12: 637-645, 2009.
43. Malach R, Reppas JB, Benson RR, Kwong KK, Jiang H, Kennedy WA, Ledden PJ, Brady TJ, Rosen BR, Tootell RB. Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. Proc Natl Acad Sci USA 92: 8135-8139, 1995.
44. Matelli M, Luppino G. Parietofrontal circuits: parallel channels for sensorymotor integrations. Adv Neurol 84: 51-61, 2000.
45. McClelland JL. On the time relations of mental processes: an examination of systems of processes in cascade. Psychol Rev 86: 287-330, 1979.
46. McPeek RM, Han JH, Keller EL. Competition between saccade goals in the superior colliculus produces saccade curvature. J Neurophysiol 89: 2577-2590, 2003.
47. McSorley E, Haggard P, Walker R. Time course of oculomotor inhibition revealed by saccade trajectory modulation. J Neurophysiol 96: 1420-1424, 2006.
48. Miller GA, Galanter E, Pribram KH. Plans and the Structure of Behavior. New York: Henry Holt, 1960.
49. Platt ML, Glimcher PW. Responses of intraparietal neurons to saccadic targets and visual distractors. J Neurophysiol 78: 1574-1589, 1997.
50. Port NL, Wurtz RH. Sequential activity of simultaneously recorded neurons in the superior colliculus during curved saccades. J Neurophysiol 90: 1887-1903, 2003.
51. Resulaj A, Kiani R, Wolpert DM, Shadlen MN. Changes of mind in decision-making. Nature 461: 263-266, 2009.
52. Rizzolatti G, Matelli M. Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153: 146-157, 2003.
53. Sailer U, Eggert T, Ditterich J, Straube A. Global effect of a nearby distractor on targeting eye and hand movements. J Exp Psychol Hum Percept Perform 28: 1432-1446, 2002.
54. Sakata H, Taira M. Parietal control of hand action. Curr Opin Neurobiol 4: 847-856, 1994.
55. 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.
56. Schall JD. Decision making: neural correlates of response time. Curr Biol 12: R800-R801, 2002a.
57. Schall JD. The neural selection and control of saccades by the frontal eye field. Philos Trans R Soc Lond B Biol Sci 357: 1073-1082, 2002b.
58. Smeets JB, Brenner E. A new view on grasping. Motor Control 3: 237-271, 1999.
59. Song JH, Nakayama K. Target selection in visual search as revealed by movement trajectories. Vision Res 48: 853-861, 2008.
60. Sternberg S. Memory-scanning: mental processes revealed by reaction-time experiments. Am Sci 57: 421-457, 1969.
61. Tipper SP, Howard DV, Houghton G. Behavioral consequences of selection from population codes. In: Attention Perform, edited by Monsell S and Driver J. Cambridge, MA: MIT Press, 2000, p. 223-245.
62. Tipper SP, Howard LA, Jackson SR. Selective reaching to grasp: evidence for distractor interference effects. Vis Cogn 4: 1-38, 1997.
63. Todd JJ, Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature 428: 751-754, 2004.
64. Todorov E. Optimality principles in sensorimotor control. Nat Neurosci 7: 907-915, 2004.
65. 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.
66. Van der Stigchel S, Meeter M, Theeuwes J. Eye movement trajectories and what they tell us. Neurosci Biobehav Rev 30: 666-679, 2006.
67. Vesia M, Prime SL, Yan X, Sergio LE, Crawford JD. Specificity of human parietal saccade and reach regions during transcranial magnetic stimulation. J Neurosci 30: 13053-13065, 2010.
68. Wang XJ. Decision making in recurrent neuronal circuits. Neuron 60: 215-234, 2008.
69. Welsh TN, Elliott D, Weeks DJ. Hand deviations toward distractors. Evidence for response competition. Exp Brain Res 127: 207-212, 1999.
70. Wood DK, Gallivan JP, Chapman CS, Milne JL, Culham JC, Goodale MA. Visual salience dominates early visuomotor competition in reaching behavior. J Vis 11: 16, 2011.
71. Woodman GF, Luck SJ. Visual search is slowed when visuospatial working memory is occupied. Psychon Bull Rev 11: 269-274, 2004.
72. Woodman GF, Vogel EK, Luck SJ. Visual search remains efficient when visual working memory is full. Psychol Sci 12: 219-224, 2001.
73. Xu Y, Chun MM. Dissociable neural mechanisms supporting visual shortterm memory for objects. Nature 440: 91-95, 2006.