Dissociable roles of right inferior frontal cortex and anterior insula in inhibitory control: Evidence from intrinsic and task-related functional parcellation, Connectivity, And response profile analyses across multiple datasets

Journal of Neuroscience

Volumn 34, Issue 44, 2014, Pages 14652-14667

  Cai, Weidong ^a   Ryali, Srikanth ^a   Chen, Tianwen ^a   Li, Chiang Shan R ^b   Menon, Vinod ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Classification; Cognitive control; Response inhibition; Stop signal task; Unsupervised learning

Indexed keywords

ANTERIOR CINGULATE; ANTERIOR INSULA; ARTICLE; BEHAVIOR; CONNECTOME; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GENERAL LINEAR MODEL; HEMODYNAMICS; HUMAN; MACHINE LEARNING; MODEL; PARIETAL CORTEX; PREFRONTAL CORTEX; STOP SIGNAL REACTION TIME; BIOLOGICAL MODEL; BRAIN CORTEX; BRAIN MAPPING; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; INHIBITION (PSYCHOLOGY); MALE; META ANALYSIS; NERVE CELL NETWORK; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; REACTION TIME;

BRAIN MAPPING; CEREBRAL CORTEX; EXECUTIVE FUNCTION; FEMALE; FRONTAL LOBE; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; NERVE NET; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; REACTION TIME;

EID: 84908325657     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3048-14.2014     Document Type: Article

References (62)

1. Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Park S, Goubert V, Hof PR (2010) The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct 214:495-517. CrossRef Medline
2. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69:e55e68. CrossRef Medline
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. CrossRef Medline
4. Aron AR, Fletcher PC, Bullmore ET, Sahakian BJ, Robbins TW (2003) Stopsignal inhibition disrupted by damage to right inferior frontal gyrus in humans. Nat Neurosci 6:115-116. CrossRef Medline
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. CrossRef Medline
6. Aron AR, Robbins TW, Poldrack RA (2014) Inhibition and the right inferior frontal cortex: one decade on. Trends Cogn Sci 18:177-185. CrossRef Medline
7. Bellec P, Rosa-Neto P, Lyttelton OC, Benali H, Evans AC (2010) Multi-level bootstrap analysis of stable clusters in resting-state fMRI. Neuroimage 51:1126-1139. CrossRef Medline
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. CrossRef Medline
9. Cai W, Leung HC (2011) Rule-guided executive control of response inhibition: functional topography of the inferior frontal cortex. PLoS One 6:e20840. CrossRef Medline
10. Cai W, Cannistraci CJ, Gore JC, Leung HC (2014) Sensorimotorindependent prefrontal activity during response inhibition. Hum Brain Mapp 35:2119-2136. CrossRef Medline
11. Carpineto C, Romano G (2012) Consensus clustering based on a new probabilistic rand index with application to subtopic retrieval. IEEE Trans Pattern Anal Mach Intell 34:2315-2326. CrossRef Medline
12. 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. CrossRef Medline
13. Chang LJ, Yarkoni T, Khaw MW, Sanfey AG (2013) Decoding the role of the insula in human cognition: functional parcellation and large-scale reverse inference. Cereb Cortex 23:739-749. CrossRef Medline
14. Chao HH, Luo X, Chang JL, Li CS (2009) Activation of the presupplementary motor area but not inferior prefrontal cortex in association with short stop signal reaction time—an intra-subject analysis. BMC Neurosci 10:75. CrossRef Medline
15. Chikazoe J, Jimura K, Asari T, Yamashita K, Morimoto H, Hirose S, Miyashita Y, Konishi S (2009) Functional dissociation in right inferior frontal cortex during performance of go/no-go task. Cereb Cortex 19:146-152. CrossRef Medline
16. Cocchi L, Harrison BJ, Pujol J, Harding IH, Fornito A, Pantelis C, Yucel M (2012) Functional alterations of large-scale brain networks related to cognitive control in obsessive-compulsive disorder. Hum Brain Mapp 33:1089-1106. CrossRef Medline
17. Cohen AL, Fair DA, Dosenbach NU, Miezin FM, Dierker D, Van Essen DC, Schlaggar BL, Petersen SE (2008) Defining functional areas in individual human brains using resting functional connectivity MRI. Neuroimage 41:45-57. CrossRef Medline
18. Cole MW, Bassett DS, Power JD, Braver TS, Petersen SE (2014) Intrinsic and task-evoked network architectures of the human brain. Neuron 83:238-251. CrossRef Medline
19. Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59-70. CrossRef Medline
20. Critchley HD, Tang J, Glaser D, Butterworth B, Dolan RJ (2005) Anterior cingulate activity during error and autonomic response. Neuroimage 27: 885-895. CrossRef Medline
21. Deen B, Pitskel NB, Pelphrey KA (2011) Three systems of insular functional connectivity identified with cluster analysis. Cereb Cortex 21:1498-1506. CrossRef Medline
22. D’Esposito M (2007) From cognitive to neural models of working memory. Philos Trans R Soc B 362:761-772. CrossRef
23. Dosenbach NU, Fair DA, Miezin FM, Cohen AL, Wenger KK, Dosenbach RA, Fox MD, Snyder AZ, Vincent JL, Raichle ME, Schlaggar BL, Petersen SE (2007) Distinct brain networks for adaptive and stable task control in humans. Proc Natl Acad Sci U S A 104:11073-11078. CrossRef Medline
24. 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. CrossRef Medline
25. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT (2009) Coordinate-based activation likelihood estimation meta-analysis of neuroimaging data: a random-effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp 30:2907-2926. CrossRef Medline
26. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT (2012) Activation likelihood estimation meta-analysis revisited. Neuroimage 59:2349-2361. CrossRef Medline
27. Erika-Florence M, Leech R, Hampshire A (2014) A functional network perspective on response inhibition and attentional control. Nat Commun 5:4073. CrossRef Medline
28. Fred ALN, Jain AK (2005) Combining multiple clusterings using evidence accumulation. IEEE Trans Pattern Anal Mach Intell 27:835-850. CrossRef Medline
29. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R (1998) Event-related fMRI: characterizing differential responses. Neuroimage 7:30-40. CrossRef Medline
30. Fuster JM (2000) Executive frontal functions. Exp Brain Res 133:66-70. CrossRef Medline
31. Garavan H, Ross TJ, Stein EA (1999) Right hemispheric dominance of inhibitory control: an event-related functional MRI study. Proc Natl Acad Sci U S A 96:8301-8306. CrossRef Medline
32. Gazzaley A, Rissman J, D’Esposito M (2004) Functional connectivity during working memory maintenance. Cogn Affect Behav Neurosci 4:580-599. CrossRef Medline
33. Glover GH, Law CS (2001) Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn Reson Med 46:515-522. CrossRef Medline
34. Goldman-Rakic PS (1995) Architecture of the prefrontal cortex and the central executive. Ann N Y Acad Sci 769:71-83. CrossRef Medline
35. Gonzalez-Castillo J, Saad ZS, Handwerker DA, Inati SJ, Brenowitz N, Bandettini PA (2012) Whole-brain, time-locked activation with simple tasks revealed using massive averaging and model-free analysis. Proc Natl Acad Sci U S A 109:5487-5492. CrossRef Medline
36. Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimer’s disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci U S A 101:4637-4642. CrossRef Medline
37. Habas C, Kamdar N, Nguyen D, Prater K, Beckmann CF, Menon V, Greicius MD (2009) Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci 29:8586-8594. CrossRef Medline
38. 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. CrossRef Medline
39. Hastie T, Tibshirani R, Friedman J (2009) The elements of statistical learning: data mining, inference, and prediction. New York: Springer.
40. Ide JS, Shenoy P, Yu AJ, Li CS (2013) Bayesian prediction and evaluation in the anterior cingulate cortex. J Neurosci 33:2039-2047. CrossRef Medline
41. 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. CrossRef Medline
42. Logan GD, Cowan WB, Davis KA (1984) On the ability to inhibit simple and choice reaction time responses: a model and a method. J Exp Psychol Hum Percept Perform 10:276-291. CrossRef Medline
43. Menon V, Uddin LQ (2010) Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct 214:655-667. CrossRef Medline
44. Miller EK, Cohen JD (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24:167-202. CrossRef Medline
45. Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MFS (2010) Cortical and subcortical interactions during action reprogramming and their related white matter pathways. Proc Natl Acad Sci U S A 107:13240-13245. CrossRef Medline
46. Orban P, Doyon J, Petrides M, Mennes M, Hoge R, Bellec P (2014) The richness of task-evoked hemodynamic responses defines a pseudohierarchy of functionally meaningful brain networks. Cereb Cortex. Advance online publication. Retrieved September 24, 2014. doi:10.1093/cercor/ bhu064. CrossRef Medline
47. Pa J, Dutt S, Mirsky JB, Heuer HW, Keselman P, Kong E, Trujillo A, Gazzaley A, Kramer JH, Seeley WW, Miller BL, Boxer AL (2014) The functional oculomotor network and saccadic cognitive control in healthy elders. Neuroimage 95C:61-68. CrossRef Medline
48. Petrides M, Pandya DN (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 16:291-310. CrossRef Medline
49. Rissman J, Gazzaley A, D’Esposito M (2004) Measuring functional connectivity during distinct stages of a cognitive task. Neuroimage 23:752-763. CrossRef Medline
50. 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. CrossRef Medline
51. 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 U S A 107: 6106-6111. CrossRef Medline
52. Smith EE, Jonides J (1998) Neuroimaging analyses of human working memory. Proc Natl Acad Sci U S A 95:12061-12068. CrossRef Medline
53. Smith SM, Fox PT, Miller KL, Glahn DC, Fox PM, Mackay CE, Filippini N, Watkins KE, Toro R, Laird AR, Beckmann CF (2009) Correspondence of the brain’s functional architecture during activation and rest. Proc Natl Acad Sci U S A 106:13040-13045. CrossRef Medline
54. Sridharan D, Levitin DJ, Menon V (2008) A critical role for the right frontoinsular cortex in switching between central-executive and default-mode networks. Proc Natl Acad Sci U S A 105:12569-12574. CrossRef Medline
55. 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. CrossRef Medline
56. 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. CrossRef Medline
57. Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, Menon V (2010) Dissociable connectivity within human angular gyrus and intraparietal sulcus: evidence from functional and structural connectivity. Cereb Cortex 20:2636-2646. CrossRef Medline
58. Uddin LQ, Supekar K, Lynch CJ, Khouzam A, Phillips J, Feinstein C, Ryali S, Menon V (2013) Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 70:869-879. CrossRef Medline
59. van den Heuvel MP, Mandl RC, Kahn RS, Hulshoff Pol HE (2009) Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum Brain Mapp 30:3127-3141. CrossRef Medline
60. Verbruggen F, Logan GD (2008) Response inhibition in the stop-signal paradigm. Trends Cogn Sci 12:418-424. CrossRef Medline
61. Xue G, Aron AR, Poldrack RA (2008) Common neural substrates for inhibition of spoken and manual responses. Cereb Cortex 18:1923-1932. CrossRef Medline
62. Zhang S, Li CS (2012) Functional networks for cognitive control in a stop signal task: independent component analysis. Hum Brain Mapp 33:89-104. CrossRef Medline