Sensorimotor-independent prefrontal activity during response inhibition

Human Brain Mapping

Volumn 35, Issue 5, 2014, Pages 2119-2136

  Cai, Weidong ^a,b   Cannistraci, Christopher J ^c   Gore, John C ^c,d   Leung, Hoi Chung ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Cognitive control; FMRI; Human; Prefrontal cortex; Stop signal task

Indexed keywords

ADULT; ARTICLE; BLOOD OXYGENATION; CONTROLLED STUDY; FEMALE; FRONTAL EYE FIELD; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; INFERIOR PARIETAL LOBULE; INHIBITION (PSYCHOLOGY); MALE; MIDDLE FRONTAL GYRUS; MIDDLE OCCIPITAL GYRUS; MIDDLE TEMPORAL GYRUS; NORMAL HUMAN; OCCIPITAL GYRUS; PREFRONTAL CORTEX; PRESUPPLEMENTARY MOTOR AREA; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RESPONSE INHIBITION; RESPONSE TIME; SACCADIC EYE MOVEMENT; SENSORIMOTOR FUNCTION; SIGNAL NOISE RATIO; SUPERIOR PARIETAL LOBULE; SUPERIOR TEMPORAL GYRUS; SUPPLEMENTARY MOTOR AREA; YOUNG ADULT; AUDITORY STIMULATION; DECISION MAKING; HEMISPHERIC DOMINANCE; IMAGE PROCESSING; MOTOR CORTEX; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; REACTION TIME;

ACOUSTIC STIMULATION; ADULT; DECISION MAKING; FEMALE; FUNCTIONAL LATERALITY; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; MOTOR CORTEX; NEUROPSYCHOLOGICAL TESTS; PHOTIC STIMULATION; PREFRONTAL CORTEX; REACTION TIME; YOUNG ADULT;

EID: 84898045359     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.22315     Document Type: Article

References (100)

1. Alexander GE, DeLong MR, Strick PL (1986): Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
2. Armstrong IT, Munoz DP (2003): Inhibitory control of eye movements during oculomotor countermanding in adults with attention-deficit hyperactivity disorder. Exp Brain Res 152:444-452.
3. Aron AR, Poldrack RA (2006): Cortical and subcortical contributions to Stop signal response inhibition: Role of the subthalamic nucleus. J Neurosci 26:2424-2433.
4. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003): Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115-116.
5. Aron AR, Behrens TE, Smith S, Frank MJ, Poldrack RA (2007): Triangulating a cognitive control network using diffusion-weighted magnetic resonance imaging (MRI) and functional MRI. J Neurosci 27:3743-3752.
6. Band GPH, van der Molen MW, Logan GD (2003): Horse-race model simulations of the stop-signal procedure. Acta Psychol 112:105-142.
7. Boecker M, Drueke B, Vorhold V, Knops A, Philippen B, Gauggel S (2011): When response inhibition is followed by response reengagement: An event-related fMRI study. Hum Brain Mapp 32:94-106.
8. Boehler CN, Appelbaum LG, Krebs RM, Hopf JM, Woldorff MG (2010): Pinning down response inhibition in the brain-conjunction analyses of the Stop-signal task. Neuroimage 52:1621-1632.
9. Boehler CN, Appelbaum LG, Krebs RM, Hopf JM, Woldorff MG (2012): The influence of different Stop-signal response time estimation procedures on behavior-behavior and brain-behavior correlations. Behav Brain Res 229:123-130.
10. Boucher L, Stuphorn V, Logan GD, Schall JD, Palmeri TJ (2007): Stopping eye and hand movements: Are the processes independent? Percept Psychophys 69:785-801.
11. Brass M, von Cramon DY (2002): The role of the frontal cortex in task preparation. Cereb Cortex 12:908-914.
12. Brown MR, Goltz HC, Vilis T, Ford KA, Everling S (2006): Inhibition and generation of saccades: Rapid event-related fMRI of prosaccades, antisaccades, and nogo trials. Neuroimage 33:644-659.
13. Brown MR, Vilis T, Everling S (2008): Isolation of saccade inhibition processes: Rapid event-related fMRI of saccades and nogo trials. Neuroimage 39:793-804.
14. Buchsbaum BR, Greer S, Chang WL, Berman KF (2005): Meta-analysis of neuroimaging studies of the Wisconsin card-sorting task and component processes. Hum Brain Mapp 25:35-45.
15. Cabel DW, Armstrong IT, Reingold E, Munoz DP (2000): Control of saccade initiation in a countermanding task using visual and auditory stop signals. Exp Brain Res 133:431-441.
16. Cai W, Leung H-C (2011): Cortical activity during manual response inhibition guided by color and orientation cues. Brain Res 1261:20-28.
17. Cai W, Leung HC (2011): Rule-guided executive control of response inhibition: Functional topography of the inferior frontal cortex. PLoS One 6:e20840.
18. Cai W, George JS, Verbruggen F, Chambers CD, Aron AR (2012): The role of the right pre-supplementary motor area in stopping action: Two studies with event-related transcranial magnetic stimulation. J Neurophysiol 108:380-389.
19. Chamberlain SR, Sahakian BJ (2007): The neuropsychiatry of impulsivity. Curr Opin Psychiatry 20:255-261.
20. Chambers CD, Bellgrove MA, Stokes MG, Henderson TR, Garavan H, Robertson IH, Morris AP, Mattingley JB (2006): Executive "brake failure" following deactivation of human frontal lobe. J Cogn Neurosci 18:444-455.
21. Chen CY, Muggleton NG, Tzeng OJ, Hung DL, Juan CH (2009): Control of prepotent responses by the superior medial frontal cortex. Neuroimage 44:537-545.
22. Chevrier AD, Noseworthy MD, Schachar R (2007): Dissociation of response inhibition and performance monitoring in the stop signal task using event-related fMRI. Hum Brain Mapp 28:1347-1358.
23. Chikazoe J, Jimura K, Asari T, Yamashita K-i, Morimoto H, Hirose S, Miyashita Y, Konishi S (2009a): Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cereb Cortex 19:146-152.
24. Chikazoe J, Jimura K, Hirose S, Yamashita K, Miyashita Y, Konishi S (2009b): Preparation to inhibit a response complements response inhibition during performance of a stop-signal task. J Neurosci 29:15870-15877.
25. Corbetta M, Shulman GL (2002): Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3:201-215.
26. Cornelissen FW, Kimmig H, Schira M, Rutschmann RM, Maguire RP, Broerse A, Den Boer JA, Greenlee MW (2002): Event-related fMRI responses in the human frontal eye fields in a randomized pro- and antisaccade task. Exp Brain Res 145:270-274.
27. Curtis CE, Cole MW, Rao VY, D'Esposito M (2005): Canceling planned action: An FMRI study of countermanding saccades. Cereb Cortex 15:1281-1289.
28. Dale AM (1999): Optimal experimental design for event-related fMRI. Hum Brain Mapp 8:109-114.
29. Derrfuss J, Brass M, von Cramon DY (2004): Cognitive control in the posterior frontolateral cortex: Evidence from common activations in task coordination, interference control, and working memory. Neuroimage 23:604-612.
30. DiQuattro NE, Geng JJ (2011): Contextual knowledge configures attentional control networks. J Neurosci 31:18026-19035.
31. Dove A, Pollmann S, Schubert T, Wiggins CJ, von Cramon DY (2000): Prefrontal cortex activation in task switching: An event-related fMRI study. Brain Res Cogn Brain Res 9:103-109.
32. Downar J, Crawley AP, Mikulis DJ, Davis KD (2001): The effect of task relevance on the cortical response to changes in visual and auditory stimuli: An event-related fMRI study. Neuroimage 14:1256-1267.
33. Downar J, Crawley AP, Mikulis DJ, Davis KD (2002): A cortical network sensitive to stimulus salience in a neutral behavioral context across multiple sensory modalities. J Neurophysiol 87:615-620.
34. Duann JR, Ide JS, Luo X, Li CS (2009): Functional connectivity delineates distinct roles of the inferior frontal cortex and presupplementary motor area in stop signal inhibition. J Neurosci 29:10171-10179.
35. Duncan J, Owen AM (2000): Common regions of the human frontal lobe recruited by diverse cognitive demands. Trends Neurosci 23:475-483.
36. Eckert MA, Menon V, Walczak A, Ahlstrom J, Denslow S, Horwitz A, Dubno JR (2009): At the heart of the ventral attention system: The right anterior insula. Hum Brain Mapp 30:2530-2541.
37. Emeric EE, Brown JW, Boucher L, Carpenter RH, Hanes DP, Harris R, Logan GD, Mashru RN, Pare M, Pouget P, Stuphorn V, Taylor TL, Schall JD (2007): Influence of history on saccade countermanding performance in humans and macaque monkeys. Vis Res 47:35-49.
38. Ettinger U, Ffytche DH, Kumari V, Kathmann N, Reuter B, Zelaya F, Williams SC (2008): Decomposing the neural correlates of antisaccade eye movements using event-related FMRI. Cereb Cortex 18:1148-1159.
39. Floden D, Stuss DT (2006): Inhibitory control is slowed in patients with right superior medial frontal damage. J Cogn Neurosci 18:1843-1849.
40. Forstmann BU, Anwander A, Schafer A, Neumann J, Brown S, Wagenmakers EJ, Bogacz R, Turner R (2010): Cortico-striatal connections predict control over speed and accuracy in perceptual decision making. Proc Natl Acad Sci USA 107:15916-15920.
41. Forstmann BU, Keuken MC, Jahfari S, Bazin PL, Neumann J, Schafer A, Anwander A, Turner R (2012): Cortico-subthalamic white matter tract strength predicts interindividual efficacy in stopping a motor response. Neuroimage 60:370-375.
42. Friston KJ (1995): Statistical parametric maps in functional imaging: A general linear approach. Hum Brain Mapp 2:189-210.
43. Friston KJ, Penny WD, Glaser DE (2005): Conjunction revisited. Neuroimage 25:661-667.
44. Funahashi S (2006): Prefrontal cortex and working memory processes. Neuroscience 139:251-261.
45. Garavan H, Ross TJ, Stein EA (1999): Right hemispheric dominance of inhibitory control: An event-related functional MRI study. Proc Natl Acad Sci USA 96:8301-8306.
46. Gaymard B, Ploner CJ, Rivaud-Pechoux S, Pierrot-Deseilligny C (1999): The frontal eye field is involved in spatial short-term memory but not in reflexive saccade inhibition. Exp Brain Res 129:288-301.
47. Geier CF, Garver KE, Luna B (2007): Circuitry underlying temporally extended spatial working memory. Neuroimage 35:904-915.
48. Groman SM, James AS, Jentsch JD (2009): Poor response inhibition: At the nexus between substance abuse and attention deficit/hyperactivity disorder. Neurosci Biobehav Rev 33:690-698.
49. Hampshire A, Chamberlain SR, Monti MM, Duncan J, Owen AM (2010): The role of the right inferior frontal gyrus: Inhibition and attentional control. Neuroimage 50:1313-1319.
50. Hanes DP, Patterson WF II, Schall JD (1998): Role of frontal eye fields in countermanding saccades: Visual, movement, and fixation activity. J Neurophysiol 79:817-834.
51. Harsay HA, Spaan M, Wijnen JG, Ridderinkhof KR (2012): Error awareness and salience processing in the oddball task: Shared neural mechanisms. Front Hum Neurosci 6:246.
52. Heinen SJ, Rowland J, Lee BT, Wade AR (2006): An oculomotor decision process revealed by functional magnetic resonance imaging. J Neurosci 26:13515-13522.
53. Hu S, Li CS (2012): Neural processes of preparatory control for stop signal inhibition. Hum Brain Mapp 33:2785-2796.
54. Ide JS, Li CS (2011): A cerebellar thalamic cortical circuit for error-related cognitive control. Neuroimage 54:455-464.
55. Ide JS, Shenoy P, Yu AJ, Li CS (2013): Bayesian prediction and evaluation in the anterior cingulate cortex. J Neurosci 33:2039-2047.
56. Jahfari S, Stinear CM, Claffey M, Verbruggen F, Aron AR (2010): Responding with restraint: What are the neurocognitive mechanisms? J Cogn Neurosci 22:1479-1492.
57. Johnstone T, Ores Walsh KS, Greischar LL, Alexander AL, Fox AS, Davidson RJ, Oakes TR (2006): Motion correction and the use of motion covariates in multiple-subject fMRI analysis. Hum Brain Mapp 27:779-788.
58. King AV, Linke J, Gass A, Hennerici MG, Tost H, Poupon C, Wessa M (2012): Microstructure of a three-way anatomical network predicts individual differences in response inhibition: A tractography study. Neuroimage 59:1949-1959.
59. Konishi S, Nakajima K, Uchida I, Kikyo H, Kameyama M, Miyashita Y (1999): Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. Brain 122(Pt 5):981-991.
60. Kornylo K, Dill N, Saenz M, Krauzlis RJ (2003): Cancelling of pursuit and saccadic eye movements in humans and monkeys. J Neurophysiol 89:2984-2999.
61. Leung H-C, Cai W (2007): Common and differential ventrolateral prefrontal activity during inhibition of hand and eye movements. J Neurosci 27:9893-9900.
62. Levy BJ, Wagner AD (2011): Cognitive control and right ventrolateral prefrontal cortex: Reflexive reorienting, motor inhibition, and action updating. Ann N Y Acad Sci 1224:40-62.
63. Levy R, Goldman-Rakic PS (2000): Segregation of working memory functions within the dorsolateral prefrontal cortex. Exp Brain Res 133:23-32.
64. Li C-s.R, Huang C, Constable RT, Sinha R (2006): Imaging response inhibition in a stop-signal task: Neural correlates independent of signal monitoring and post-response processing. J Neurosci 26:186-192.
65. Li C-sR, Yan P, Sinha R, Lee T-W (2008): Subcortical processes of motor response inhibition during a stop signal task. Neuroimage 41:1352-1363.
66. Liu X, Banich MT, Jacobson BL, Tanabe JL (2004): Common and distinct neural substrates of attentional control in an integrated Simon and spatial Stroop task as assessed by event-related fMRI. Neuroimage 22:1097-1106.
67. Logan GD, Cowan WB (1984): On the ability to inhibit thought and action: A theory of an act of control. Psychol Rev 91:195-327.
68. Luks TL, Simpson GV, Dale CL, Hough MG (2007): Preparatory allocation of attention and adjustments in conflict processing. Neuroimage 35:949-958.
69. Makino Y, Yokosawa K, Takeda Y, Kumada T (2004): Visual search and memory search engage extensive overlapping cerebral cortices: An fMRI study. Neuroimage 23:525-533.
70. Metereau E, Dreher JC: Cerebral correlates of salient prediction error for different rewards and punishments. Cereb Cortex (in press).
71. Morein-Zamir S, Kingstone A (2006): Fixation offset and stop signal intensity effects on saccadic countermanding: A crossmodal investigation. Exp Brain Res 175:453-462.
72. Mort DJ, Perry RJ, Mannan SK, Hodgson TL, Anderson E, Quest R, McRobbie D, McBride A, Husain M, Kennard C (2003): Differential cortical activation during voluntary and reflexive saccades in man. Neuroimage 18:231-246.
73. Munoz DP, Wurtz RH (1993): Fixation cells in monkey superior colliculus. I. Characteristics of cell discharge. J Neurophysiol 70:559-575.
74. Munoz DP, Wurtz RH (1995): Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol 73:2313-2333.
75. Nachev P, Wydell H, O'Neill K, Husain M, Kennard C (2007): The role of the pre-supplementary motor area in the control of action. Neuroimage 36 Suppl 2:T155-163.
76. Nee DE, Wager TD, Jonides J (2007): Interference resolution: Insights from a meta-analysis of neuroimaging tasks. Cogn Affect Behav Neurosci 7:1-17.
77. Nelson SM, Dosenbach NU, Cohen AL, Wheeler ME, Schlaggar BL, Petersen SE (2010): Role of the anterior insula in task-level control and focal attention. Brain Struct Funct 214:669-680.
78. Neumann J, von Cramon DY, Lohmann G (2008): Model-based clustering of meta-analytic functional imaging data. Hum Brain Mapp 29:177-192.
79. Nichols T, Brett M, Andersson J, Wager T, Poline J-B (2005): Valid conjunction inference with the minimum statistic. Neuroimage 25:653-660.
80. Pare M, Hanes DP (2003): Controlled movement processing: Superior colliculus activity associated with countermanded saccades. J Neurosci 23:6480-6489.
81. Petrides M (2000): The role of the mid-dorsolateral prefrontal cortex in working memory. Exp Brain Res 133:44-54.
82. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004): The role of the medial frontal cortex in cognitive control. Science 306:443-447.
83. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, Simmons A, Williams SC, Giampietro V, Andrew CM, Taylor E (2001): Mapping motor inhibition: Conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13:250-261.
84. Rushworth MF, Hadland KA, Paus T, Sipila PK (2002): Role of the human medial frontal cortex in task switching: A combined fMRI and TMS study. J Neurophysiol 87:2577-2592.
85. Rushworth MF, Walton ME, Kennerley SW, Bannerman DM (2004): Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:410-417.
86. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, Greicius MD (2007): Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349-2356.
87. Sharp DJ, Bonnelle V, De Boissezon X, Beckmann CF, James SG, Patel MC, Mehta MA (2010): Distinct frontal systems for response inhibition, attentional capture, and error processing. Proc Natl Acad Sci USA 107:6106-6111.
88. Simmonds DJ, Pekar JJ, Mostofsky SH (2008): Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia 46:224-232.
89. Stuphorn V, Schall JD (2006): Executive control of countermanding saccades by the supplementary eye field. Nat Neurosci 9:925-931.
90. Stuphorn V, Taylor TL, Schall JD (2000): Performance monitoring by the supplementary eye field. Nature 408:857-860.
91. Swann NC, Cai W, Conner CR, Pieters TA, Claffey MP, George JS, Aron AR, Tandon N (2012): Roles for the pre-supplementary motor area and the right inferior frontal gyrus in stopping action: Electrophysiological responses and functional and structural connectivity. Neuroimage 59:2860-2870.
92. Swick D, Ashley V, Turken U (2011): Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks. Neuroimage 56:1655-1665.
93. Tabu H, Mima T, Aso T, Takahashi R, Fukuyama H (2012): Common inhibitory prefrontal activation during inhibition of hand and foot responses. Neuroimage 59:3373-3378.
94. Verbruggen F, Logan GD (2008): Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12:418-424.
95. Wager TD, Sylvester CY, Lacey SC, Nee DE, Franklin M, Jonides J (2005): Common and unique components of response inhibition revealed by fMRI. Neuroimage 27:323-340.
96. Walker R, Walker DG, Husain M, Kennard C (2000): Control of voluntary and reflexive saccades. Exp Brain Res 130:540-544.
97. Wiech K, Lin CS, Brodersen KH, Bingel U, Ploner M, Tracey I (2010): Anterior insula integrates information about salience into perceptual decisions about pain. J Neurosci 30:16324-16331.
98. Xue G, Aron, AR, Poldrack RA (2008): Common neural substrates for inhibition of spoken and manual responses. Cereb Cortex 18:1923-1932.
99. Zhang S, Li CS (2012): Functional networks for cognitive control in a stop signal task: Independent component analysis. Hum Brain Mapp 33:89-104.
100. Zhang S, Ide JS, Li CS (2012): Resting-state functional connectivity of the medial superior frontal cortex. Cereb Cortex 22:99-111.