Human visual and parietal cortex encode visual choices independent of motor plans

NeuroImage

Volumn 63, Issue 3, 2012, Pages 1393-1403

  Hebart, Martin N ^a,b   Donner, Tobias H ^c   Haynes, John Dylan ^a,b,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF AMSTERDAM   (Netherlands)

^d MAX PLANCK INSTITUTE FOR HUMAN COGNITIVE AND BRAIN SCIENCES   (Germany)

Author keywords

Decision making; Decoding; FMRI; Motion perception; Multivoxel pattern analysis; Signal detection theory

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DECISION MAKING; ELECTROENCEPHALOGRAM; EYE TRACKING; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; MALE; MOTOR ACTIVITY; MOTOR PLANNING; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; PARIETAL CORTEX; PRIORITY JOURNAL; STIMULUS RESPONSE; VISUAL CORTEX;

ADULT; BRAIN MAPPING; CHOICE BEHAVIOR; FEMALE; HUMANS; IMAGE INTERPRETATION, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MOTION PERCEPTION; PARIETAL LOBE; VISUAL CORTEX; YOUNG ADULT;

EID: 84866148333     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2012.08.027     Document Type: Article

References (80)

1. Apthorp The role of motion streaks in human visual motion perception Available at, [Accessed June 15, 2012]. http://ses.library.usyd.edu.au/bitstream/2123/7432/1/dm-apthorp-2011-thesis.pdf.
2. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
3. Bankó E.M., Gál V., Körtvélyes J., Kovács G., Vidnyánszky Z. Dissociating the effect of noise on sensory processing and overall decision difficulty. J. Neurosci. 2011, 31:2663-2674.
4. Bennur S., Gold J.I. Distinct representations of a perceptual decision and the associated oculomotor plan in the monkey lateral intraparietal area. J. Neurosci. 2011, 31:913-921.
5. Bode S., Haynes J.-D. Decoding sequential stages of task preparation in the human brain. Neuroimage 2009, 45:606-613.
6. Bogacz R., Brown E., Moehlis J., Holmes P., Cohen J.D. The physics of optimal decision making: a formal analysis of models of performance in two-alternative forced-choice tasks. Psychol. Rev. 2006, 113:700-765.
7. Born R.T., Bradley D.C. Structure and function of visual area MT. Annu. Rev. Neurosci. 2005, 28:157-189.
8. Botvinick M.M., Cohen J.D., Carter C.S. Conflict monitoring and anterior cingulate cortex: an update. Trends Cogn. Sci. 2004, 8:539-546.
9. Braddick O.J., O'Brien J.M.D., Wattam-Bell J., Atkinson J., Hartley T., Turner R. Brain areas sensitive to coherent visual motion. Perception 2001, 30:61-72.
10. Britten K.H., Newsome W.T., Shadlen M.N., Celebrini S., Movshon J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 1996, 13:87-100.
11. Chang C.C., Lin C.J. LIBSVM: a library for support vector machines. ACM Trans. Intell. Syst. Technol. 2011, 2:1-27.
12. Cisek P., Kalaska J.F. Neural correlates of reaching decisions in dorsal premotor cortex: specification of multiple direction choices and final selection of action. Neuron 2005, 45:801-814.
13. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
14. Culham J.C., Cavina-Pratesi C., Singhal A. The role of parietal cortex in visuomotor control: what have we learned from neuroimaging?. Neuropsychologia 2006, 44:2668-2684.
15. Dale A.M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 1999, 8:109-114.
16. Dehaene S., Spelke E., Pinel P., Stanescu R., Tsivkin S. Sources of mathematical thinking: behavioral and brain-imaging evidence. Science 1999, 284:970-974.
17. Domenech P., Dreher J.C. Decision threshold modulation in the human brain. J. Neurosci. 2010, 30:14305-14317.
18. Donner T.H., Siegel M., Fries P., Engel A.K. Buildup of choice-predictive activity in human motor cortex during perceptual decision making. Curr. Biol. 2009, 19:1581-1585.
19. Dumoulin S.O., Bittar R.G., Kabani N.J., Baker C.L., Le Goualher G., Pike G.B., Evans A.C. A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb. Cortex 2000, 10:454-463.
20. Freedman D.J., Assad J.A. A proposed common neural mechanism for categorization and perceptual decisions. Nat. Neurosci. 2011, 14:143-146.
21. Friston K. A theory of cortical responses. Philos. Trans. R Soc. B: Biol. Sci. 2005, 360:815-836.
22. Gold J.I., Shadlen M.N. Representation of a perceptual decision in developing oculomotor commands. Nature 2000, 404:390-394.
23. Gold J.I., Shadlen M.N. The influence of behavioral context on the representation of a perceptual decision in developing oculomotor commands. J. Neurosci. 2003, 23:632-651.
24. Gold J.I., Shadlen M.N. The neural basis of decision making. Annu. Rev. Neurosci. 2007, 30:535-574.
25. Grinband J., Hirsch J., Ferrera V.P. A neural representation of categorization uncertainty in the human brain. Neuron 2006, 49:757-763.
26. Hanks T.D., Ditterich J., Shadlen M.N. Microstimulation of macaque area LIP affects decision-making in a motion discrimination task. Nat. Neurosci. 2006, 9:682-689.
27. Haynes J.-D., Sakai K., Rees G., Gilbert S., Frith C., Passingham R.E. Reading hidden intentions in the human brain. Curr. Biol. 2007, 17:323-328.
28. Heekeren H.R., Marrett S., Bandettini P.A., Ungerleider L.G. A general mechanism for perceptual decision-making in the human brain. Nature 2004, 431:859-862.
29. Heekeren H.R., Marrett S., Ruff D.A., Bandettini P.A., Ungerleider L.G. Involvement of human left dorsolateral prefrontal cortex in perceptual decision making is independent of response modality. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:10023-10028.
30. Heekeren H.R., Marrett S., Ungerleider L.G. The neural systems that mediate human perceptual decision making. Nat. Rev. Neurosci. 2008, 9:467-479.
31. Hesselmann G., Kell C.A., Eger E., Kleinschmidt A. Spontaneous local variations in ongoing neural activity bias perceptual decisions. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10984-10989.
32. Hesselmann G., Kell C.A., Kleinschmidt A. Ongoing activity fluctuations in hMT+ bias the perception of coherent visual motion. J. Neurosci. 2008, 28:14481-14485.
33. Ho T.C., Brown S., Serences J.T. Domain general mechanisms of perceptual decision making in human cortex. J. Neurosci. 2009, 29:8675-8687.
34. Horwitz G.D., Newsome W.T. Separate signals for target selection and movement specification in the superior colliculus. Science 1999, 284:1158-1161.
35. Horwitz G.D., Batista A.P., Newsome W.T. Representation of an abstract perceptual decision in macaque superior colliculus. J. Neurophysiol. 2004, 91:2281-2296.
36. Kahnt T., Heinzle J., Park S.Q., Haynes J.-D. The neural code of reward anticipation in human orbitofrontal cortex. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:6010-6015.
37. Kamitani Y., Tong F. Decoding seen and attended motion directions from activity in the human visual cortex. Curr. Biol. 2006, 16:1096-1102.
38. Kayser A.S., Buchsbaum B.R., Erickson D.T., D'Esposito M. The functional anatomy of a perceptual decision in the human brain. J. Neurophysiol. 2010, 103:1179-1194.
39. Kayser A.S., Erickson D.T., Buchsbaum B.R., D'Esposito M. Neural representations of relevant and irrelevant features in perceptual decision making. J. Neurosci. 2010, 30:15778-15789.
40. Kiani R., Shadlen M.N. Representation of confidence associated with a decision by neurons in the parietal cortex. Science 2009, 324:759-764.
41. Kim J.-N., Shadlen M.N. Neural correlates of a decision in the dorsolateral prefrontal cortex of the macaque. Nat. Neurosci. 1999, 2:176-185.
42. Kovács G., Cziraki C., Greenlee M.W. Neural correlates of stimulus invariant decisions about motion in depth. Neuroimage 2010, 51:329-335.
43. Kriegeskorte N., Goebel R., Bandettini P. Information-based functional brain mapping. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:3863-3868.
44. Li S., Mayhew S., Kourtzi Z. Learning shapes the representation of behavioral choice in the human brain. Neuron 2009, 62:441-452.
45. Liu T., Pleskac T.J. Neural correlates of evidence accumulation in a perceptual decision task. J. Neurophysiol. 2011, 106:2383-2398.
46. Mazurek M.E., Roitman J.D., Ditterich J., Shadlen M.N. A role for neural integrators in perceptual decision making. Cereb. Cortex 2003, 13:1257-1269.
47. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
48. Nienborg H., Cumming B.G. Decision-related activity in sensory neurons reflects more than a neuron's causal effect. Nature 2009, 459:89-92.
49. Noppeney U., Ostwald D., Werner S. Perceptual decisions formed by accumulation of audiovisual evidence in prefrontal cortex. J. Neurosci. 2010, 30:7434-7446.
50. O'Regan J.K., Noë A. A sensorimotor account of vision and visual consciousness. Behav. Brain Sci. 2001, 24:939-973.
51. Pessoa L., Kastner S., Ungerleider L.G. Neuroimaging studies of attention: from modulation of sensory processing to top-down control. J. Neurosci. 2003, 23:3990-3998.
52. Philiastides M.G., Sajda P. Temporal characterization of the neural correlates of perceptual decision making in the human brain. Cereb. Cortex 2006, 16:509-518.
53. Ploran E.J., Nelson S.M.M., Velanova K., Donaldson D.I., Petersen S.E., Wheeler M.E. Evidence accumulation and the moment of recognition: dissociating decision processes using fMRI. J. Neurosci. 2007, 27:11912-11924.
54. Price C.J. The anatomy of language: contributions from functional neuroimaging. J. Anat. 2000, 197:335-359.
55. Rahnev D., Lau H., de Lange F.P. Prior expectation modulates the interaction between sensory and prefrontal regions in the human brain. J. Neurosci. 2011, 31:10741-10748.
56. Ratcliff R. A theory of memory retrieval. Psychol. Rev. 1978, 85:59-108.
57. Rees G., Friston K., Koch C. A direct quantitative relationship between the functional properties of human and macaque V5. Nat. Neurosci. 2000, 3:716-723.
58. Ridderinkhof R.R., Ullsperger M., Crone E.A., Nieuwenhuis S. The role of the medial frontal cortex in cognitive control. Science 2004, 306:443-447.
59. Roitman J.D., Shadlen M.N. Response of neurons in the lateral intraparietal area during a combined visual discrimination reaction time task. J. Neurosci. 2002, 22:9475-9489.
60. Romo R., Hernández A., Zainos A., Lemus L., Brody C. Neuronal correlates of decision-making in secondary somatosensory cortex. Nat. Neurosci. 2002, 5:1217-1225.
61. Sakai K., Passingham R.E. Prefrontal set activity predicts rule-specific neural processing during subsequent cognitive performance. J. Neurosci. 2006, 26:1211-1218.
62. Salinas E., Romo R. Conversion of sensory signals into motor commands in primary motor cortex. J. Neurosci. 1998, 18:499-511.
63. Salinas E., Hernández A., Zainos A., Romo R. Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli. J. Neurosci. 2000, 20:5503-5515.
64. Serences J.T., Boynton G.M. Feature-based attentional modulations in the absence of direct visual stimulation. Neuron 2007, 55:301-312.
65. Serences J.T., Boynton G.M. The representation of behavioral choice for motion in human visual cortex. J. Neurosci. 2007, 27:12893-12899.
66. Shadlen M.N., Newsome W.T. Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. J. Neurophysiol. 2001, 86:1916-1936.
67. Shadlen M.N., Kiani R., Hanks T.D., Churchland A.K. Neurobiology of decision making: An intentional framework. Better Than Conscious? Decision Making, the Human Mind, and Implications For Institutions 2008, 71-101. The MIT Press, Cambridge. C. Engel, W. Singer (Eds.).
68. Silver M.A., Kastner S. Topographic maps in human frontal and parietal cortex. Trends Cogn. Sci. 2009, 13:488-495.
69. Singh K.D., Fawcett I.P. Transient and linearly graded deactivation of the human default-mode network by a visual detection task. Neuroimage 2008, 41:100-112.
70. Swisher J.D., Halko M.A., Merabet L.B., McMains S.A., Somers D.C. Visual topography of human intraparietal sulcus. J. Neurosci. 2007, 27:5326-5337.
71. Tosoni A., Galati G., Luca G., Corbetta M. Sensory-motor mechanisms in human parietal cortex underlie arbitrary visual decisions. Nat. Neurosci. 2008, 11:1446-1453.
72. Treue S. Visual attention: the where, what, how and why of saliency. Curr. Opin. Neurobiol. 2003, 13:428-432.
73. Troxler I.P. Über das Verschwinden gegebener Gegenstände innerhalb unseres Gesichtskreises. Ophthalmol. Bibliothek 1804, 2:1-53.
74. Tusche A., Bode S., Haynes J.-D. Neural responses to unattended products predict later consumer choices. J. Neurosci. 2010, 30:8024-8031.
75. Uchida N., Kepecs A., Mainen Z.F. Seeing at a glance, smelling in a whiff: rapid forms of perceptual decision making. Nat. Rev. Neurosci. 2006, 7:485-491.
76. Usher M., McClelland J.L. The time course of perceptual choice: the leaky, competing accumulator model. Psychol. Rev. 2001, 108:550-592.
77. Watson A.B., Pelli D.G. QUEST: a Bayesian adaptive psychometric method. Percept. Psychophys. 1983, 33:113-120.
78. Woolgar A., Hampshire A., Thompson R., Duncan J. Adaptive coding of task-relevant information in human frontoparietal cortex. J. Neurosci. 2011, 31:14592-14599.
79. Wyart V., Tallon-Baudry C. How ongoing fluctuations in human visual cortex predict perceptual awareness: baseline shift versus decision bias. J. Neurosci. 2009, 29:8715-8725.
80. Zeki S.M. Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol. 1974, 236:549-573.