Linear age-correlated functional development of right inferior fronto-striato-cerebellar networks during response inhibition and anterior cingulate during error-related processes

Human Brain Mapping

Volumn 28, Issue 11, 2007, Pages 1163-1177

  Rubia, Katya ^a   Smith, Anna B ^a   Taylor, Eric ^a   Brammer, Michael ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Cognitive control; Cognitive neuroscience; Development; Executive functions; fMRI; Motor inhibition

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; BASAL GANGLION; BRAIN REGION; CEREBELLUM; CEREBELLUM CORTEX; CHILD; CINGULATE GYRUS; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATION ANALYSIS; ELECTROENCEPHALOGRAM; ERROR; FRONTAL LOBE; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; INHIBITION KINETICS; MALE; MOTOR PERFORMANCE; NERVE CELL DIFFERENTIATION; NEUROIMAGING; NORMAL HUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; TASK PERFORMANCE; THALAMUS;

ADOLESCENT; ADULT; AGING; BRAIN; BRAIN MAPPING; CEREBELLUM; CHILD; COGNITION; CORPUS STRIATUM; FUNCTIONAL LATERALITY; GYRUS CINGULI; HUMANS; JUDGMENT; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PREFRONTAL CORTEX; THALAMUS; VOLITION;

EID: 35948949386     PISSN: 10659471     EISSN: None     Source Type: Journal    
DOI: 10.1002/hbm.20347     Document Type: Article

References (90)

1. Adleman NE, Menon V, Blasey CM, White CD, Warsofsky IS, Glover GH, Reiss AL (2002): A developmental fMRI study of the stroop color-word task. Neuroimage 16:61-75.
2. Alexander GE, DeLong MR, Strick PL (1986): Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
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 (Vol. 6, pp 115, 2003). Nat Neurosci 6:1329-1329.
5. Benjamini Y, Hochberg Y (1995): Controlling the false discovery rate - A practical and powerful approach to multiple testing. J R Stat Soc B Met 57:289-300.
6. Bjorklund DF, Harnishfeger KK (1990): The resources construct in cognitive-development - Diverse sources of evidence and a theory of inefficient inhibition. Dev Rev 10:48-71.
7. Booth JR, Burman DD, Meyer JR, Lei Z, Trommer BL, Davenport ND, Li W, Parrish TB, Gitelman DR, Mesulam MM (2003): Neural development of selective attention and response inhibition. Neuroimage 20:737-751.
8. Botvinick M, Nystrom LE, Fissell K, Carter CS, Cohen JD (1999): Conflict monitoring versus selection-for-action in anterior cingulate cortex. Nature 402:179-181.
9. Brammer MJ, Bullmore ET, Simmons A, Williams SC, Grasby PM, Howard RJ, Woodruff PW, Rabe-Hesketh S (1997): Generic brain activation mapping in functional magnetic resonance imaging: A nonparametric approach. Magn Reson Imaging 15:763-770.
10. Braver TS, Barch DM, Gray JR, Molfese DL, Snyder A (2001): Anterior cingulate cortex and response conflict: Effects of frequency, inhibition and errors. Cereb Cortex 11:825-836.
11. Brown TT, Lugar HM, Coalson RS, Miezin FM, Petersen SE, Schlaggar BL (2005): Developmental changes in human cerebral functional organization for word generation. Cereb Cortex 15:275-290.
12. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ (1999): Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans Med Imaging 18:32-42.
13. Bullmore E, Long C, Suckling J, Fadili J, Calvert G, Zelaya F, Carpenter TA, Brammer M (2001): Colored noise and computational inference in neurophysiological (fMRI) time series analysis: Resampling methods in time and wavelet domains. Hum Brain Mapp 12:61-78.
14. Bunge SA, Dudukovic NM, Thomason ME, Vaidya CJ, Gabrieli JDE (2002): Immature frontal lobe contributions to cognitive control in children: Evidence from fMRI. Neuron 33:301-311.
15. Burrock MA, Buckner RL, Woldorff MG, Rosen BR, Dale A (1998): Randomised event-related experimental designs allow for extremely rapid presentation rates using functional MRI. Neuroreport 9:3735-3739.
16. Carter C, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998): Anterior cingulate cortex, error detection and the online monitoring of performance. Science 280:747-749.
17. Carter CS, Botvinick MM, Cohen JD (1999): The contribution of the anterior cingulate cortex to executive processes in cognition. Rev Neurosci 10:49-57.
18. Carter CS, Macdonald AM, Botvinick M, Ross LL, Stenger VA, Noll D, Cohen JD (2000): Parsing executive processes: Strategic vs. evaluative functions of the anterior cingulate cortex. Proc Natl Acad Sci USA 97:1944-1948.
19. Casey BJ, Trainor RJ, Orendi JL, Schubert AB, Nystrom LE, Giedd JN, Castellanos FX, Haxby JV, Noll DC, Cohen JD, Forman SD, Dahl RE, Rapoport JL (1997): A developmental functional MRI study of prefrontal activation during performance of a Go-No-Go task. J Cogn Neurosci 9:835-847.
20. Casey BJ, Thomas KM, Davidson MC, Kunz K, Franzen PL (2002): Dissociating striatal and hippocampal function developmentally with a stimulus-response compatibility task. J Neurosci 22:8647-8652.
21. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, Blumenthal JD, James RS, Ebens CL, Walter JM, Zijdenbos A, Evans AC, Giedd JN, Rapoport JL (2002): Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder. JAMA 288:1740-1748.
22. 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 Neurosc 18:444-455.
23. Changeux JP, Danchin A (1976): Selective stabilization of developing synapses as a mechanism for specification of neuronal networks. Nature 264:705-712.
24. Critchley H, Daly E, Phillips M, Brammer M, Bullmore E, Williams S, Van Amelsvoort T, Robertson D, David A, Murphy D (2000): Explicit and implicit neural mechanisms for processing of social information from facial expressions: A functional magnetic resonance imaging study. Hum Brain Mapp 9:93-105.
25. Dale AM (1999): Optimal design for event-related fMRI. Hum Brain Mapp 8:109-114.
26. Dale AM, Buckner RL (1997): Selected averaging of rapidly presented individual trials using fMRI. Hum Brain Mapp 5:329-340.
27. Davies PL, Segalowitz SJ, Gavin WJ (2004a): Development of error-monitoring event-related potentials in adolescents. Ann N Y Acad Sci 1021:324-328.
28. Davies PL, Segalowitz SJ, Gavin WJ (2004b): Development of response-monitoring ERPs in 7-to 25-year-olds. Dev Neuropsychol 25:355-376.
29. Dempster FN (1992): The rise and fall of the inhibitory mechanism - Toward a unified theory of cognitive-development and aging. Dev Rev 12:45-75.
30. Durston S, Casey BJ (2006): What have we learned about cognitive development from neuroimaging? Neuropsychologia 44:2149-2157.
31. Durston S, Thomas KM, Yang YH, Ulug AM, Zimmerman RD, Casey BJ (2002a): A neural basis for the development of inhibitory control. Dev Sci 5:F9-F16.
32. Durston S, Thomas KM, Worden MS, Yang Y, Casey BJ (2002b): The effect of preceding context on inhibition: An event-related fMRI study. Neuroimage 16:449-453.
33. Durston S, Davidson M, Tottenham N, Galvan A, Spicer J, Fossella JA, Casey BJ (2006): A shift from diffuse to focal brain activation during development. Dev Sci 5:F9-F16.
34. Fellows LK, Farah MJ (2005): Is anterior cingulate cortex necessary for cognitive control? Brain 128:788-796.
35. Fiehler K, Ullsperger M, von Cramon DY (2004): Neural correlates of error detection and error correction: Is there a common neuroanatomical substrate? Eur J Neurosci 19:3081-3087.
36. 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.
37. Garavan H, Ross TJ, Murphy K, Roche RAP, Stein EA (2002): Dissociable executive functions in the dynamic control of behavior: Inhibition, error detection, and correction. Neuroimage 17:1820-1829.
38. Garavan H, Ross TJ, Kaufman J, Stein EA (2003): A midline dissociation between error-processing and response-conflict monitoring. Neuroimage 20:1132-1139.
39. Giedd JN, Blumenthal J, Jeffries NO, Castellanos FX, Liu H, Zijdenbos A, Paus T, Evans AC, Rapoport JL (1999): Brain development during childhood and adolescence: A longitudinal MRI study. Nat Neurosci 2:861-863.
40. Godefroy O, Lhullier C, Rousseaux M (1996): Non-spatial attention disorders in patients with frontal or posterior brain damage. Brain 119:191-202.
41. Gogtay N, Giedd JN, Lusk L, Hayashi KM, Greenstein D, Vaituzis AC, Nugent TF, Herman DH, Clasen LS, Toga AW, Rapoport IL, Thompson PM (2004): Dynamic mapping of human cortical development during childhood through early adulthood. Proc Natl Acad Sci USA 101:8174-8179.
42. Grossman M, Cooke A, DeVita C, Alsop D, Detre J, Chen W, Gee J (2002): Age-related changes in working memory during sentence comprehension: An fMRI study. Neuroimage 15:302-317.
43. Hester R, Fassbender C, Garavan H (2004): Individual differences in error processing: A review and reanalysis of three event-related fMRI studies using the GO/NOGO task. Cereb Cortex 14:986-994.
44. Huttenlocher PR, Dabholkar AS (1997): Regional differences in synaptogenesis in human cerebral cortex. J Comp Neurol 387:167-178.
45. Jones LB, Rothbart MK, Posner MI (2003): Development of executive attention in preschool children. Dev Sci 6:498-504.
46. Kawashima R, Satoh K, Itoh H, Ono S, Furumoto S, Gotoh R, Koyama M, Yoshioka S, Takahashi T, Takahashi K, Yanagisawa T, Fukuda H (1996): Functional anatomy of go/no-go discrimination and response selection - A pet study in man. Brain Res 728:79-89.
47. Kelly AMC, Hester R, Murphy K, Javitt DC, Foxe JJ, Garavan H (2004): Prefrontal-subcortical dissociations underlying inhibitory control revealed by event-related fMRI. Eur J Neurosci 19:3105-3112.
48. Kim SG, Ugurbil K, Strick PL (1994): Activation of a cerebellar output nucleus during cognitive processing. Science 265:949-951.
49. Konishi S, Nakajima K, Uchida I, Sekihara K, Miyashita Y (1998): No-go dominant brain activity in human inferior prefrontal cortex revealed by functional magnetic resonance imaging. Eur J Neurosci 10:1209-1213.
50. Ladouceur CD, Dahl RE, Carter CS (2004): ERP correlates of action monitoring in adolescence. Adolescent brain development: Vulnerabilities and opportunities. Ann N Y Acad Sci 1021:329-336.
51. Levin HS, Culhane KA, Hartmann J, Evankovich K, Mattson AJ, Harward H, Ringholz G, Ewingcobbs L, Fletcher JM (1991): Developmental-changes in performance on tests of purported frontal-lobe functioning. Dev Neuropsychol 7:377-395.
52. Liddle PF, Kiehl KA, Smith AM (2001): Event-related fMRI study of response inhibition. Hum Brain Mapp 12:100-109.
53. Liston C, Watts R, Tottenham N, Davidson MC, Niogi S, Ulug AM, Casey BJ (2005): Fronto-striatal microstructure modulates efficient recruitment of cognitive control. Cereb Cortex 16:553-560.
54. Logan GD, Schachar RJ, Tannock R (1997): Impulsivity and inhibitory control. Psychol Sci 8:60-64.
55. Luna B, Thulborn KR, Munoz DP, Merriam EP, Garver KE, Minshew NI, Keshavan MS, Genovese CR, Eddy WF, Sweeney IA (2001): Maturation of widely distributed brain function subserves cognitive development. Neuroimage 13:786-793.
56. Menon V, Adleman NE, White CD, Glover GH, Reiss AL (2001): Error-related brain activation during a Go/NoGo response inhibition task. Hum Brain Mapp 12:131-143.
57. Mesulam MM, Nobre AC, Kim YH, Parrish TB, Gitelman DR (2001): Heterogeneity of cingulate contributions to spatial attention. Neuroimage 13:1065-1072.
58. Middleton FA, Strick PL (2000): Basal ganglia and cerebellar loops: Motor and cognitive circuits. Brain Res Rev 31:236-250.
59. Mostofsky SH, Schafer JGB, Abrams MT, Goldberg MC, Flower AA, Boyce A, Courtney SM, Calhoun VD, Kraut MA, Denckla MB, Pekar JJ (2003): fMRI evidence that the neural basis of response inhibition is task-dependent. Cogn Brain Res 17:419-430.
60. Murphy K, Garavan H (2004): An empirical investigation into the number of subjects required for an event-related fMRI study. Neuroimage 22:879-885.
61. Nosarti C, Rubia K, Smith A, Frearson S, Williams S, Rifkin L, Murray R (2006): Altered functional neuroanatomy of response inhibition in adolescent boys who were born very preterm. Dev Med Child Neurol 48:265-271.
62. Paus T, Zijdenbos A, Worsley K, Collins DL, Blumenthal J, Giedd JN, Rapoport JL, Evans AC (1999): Structural maturation of neural pathways in children and adolescents: In vivo study. Science 283:1908-1911.
63. Petersen B, Vohr B, Kane M, Whalen D, Schneider K, Katz K, Zhang H, Duncan C, Makuch R, Gore C, Ment L (2002): A functional magnetic resonance imaging study of language processing and its cognitive correlates in prematurely born children. Pediatrics 110:1153-1162.
64. Raven J 1960: Guide to the Standard Progressive Matrices. London: HK Lewis.
65. Ridderinkhof KR, Ullsperger M, Crone EA, Nieuwenhuis S (2004): The role of the medial frontal cortex in cognitive control. Science 15:443-447.
66. Rieger M, Gauggel S, Burmeister K (2003): Inhibition of ongoing responses following frontal, nonfrontal, and basal ganglia lesions. Neuropsychology 17:272-282.
67. Rubia K (2002): The dynamic approach to neurodevelopmental psychiatric disorders: Use of fMRI combined with neuropsychology to elucidate the dynamics of psychiatric disorders, exemplified in ADHD and schizophrenia. Behav Brain Res 130:47-56.
68. Rubia K, Oosterlaan J, Sergeant JA, Brandeis D, von Leeuwen T (1998a): Inhibitory dysfunction in hyperactive boys. Behav Brain Res 94:25-32.
69. Rubia K, Overmeyer S, Taylor E, Brammer M, Williams S, Simmons A, Andrew C, Bullmore E (1998b): Prefrontal involvement in "temporal bridging" and timing movement. Neuropsychologia 36:1283-1293.
70. Rubia K, Overmeyer S, Taylor E, Brammer M, Williams SCR, Simmons A, Bullmore E (1999): Hypofrontality in attention deficit hyperactivity disorder ADHD during higher-order motor control: A study using fMRI. Am J Psychiatry 156:891-896.
71. Rubia K, Overmeyer S, Taylor E, Brammer M, Williams S, Simmons A, Andrew C, Bullmore E (2000): Functional frontalisation with age: Mapping neurodevelopmental trajectories with fMRI. Neurosci Biobehav Rev 24:13-19.
72. Rubia K, Russell T, Overmeyer S, Brammer MJ, Bullmore ET, Sharma T, Simmons A, Williams SCR, Giampietro V, Andrew CM, et al. (2001): Mapping motor inhibition: Conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13:250-261.
73. Rubia K, Smith AB, Brammer MJ, Taylor E (2003): Right inferior prefrontal cortex mediates response inhibition while mesial prefrontal cortex is responsible for error detection. Neuroimage 20:351-358.
74. Rubia K, Lee F, Cleare A, Tunstall N, Fu C, McGuire P (2005a): Acute tryptophan depletion reduces right inferior prefrontal activation during response inhibition in fast, event related fMRI. Psychopharmacology 179:791-801.
75. Rubia K, Smith AB, Brammer M, Toone B, Taylor E (2005b): Medication-naïve adolescents with attention-deficit hyperactivity disorder show abnormal brain activation during inhibition and error detection. Am J Psychiatry 162:1067-1075.
76. Rubia K, Smith A, Taylor E (2007): Performance of children with attention deficit hyperactivity disorder (ADHD) on a test battery for impulsiveness. Child Neuropsychology 13:276-304.
77. Rubia K, Smith AB, Woolley J, Nosarti C, Heyman I, Taylor E, Brammer MJ (2006): Progressive increase of fronto-striatal brain activation from childhood to adulthood during event related tasks of cognitive control. Hum Brain Mapp 27:973-993.
78. Schlaggar BL, Brown TT, Lugar HM, Visscher KM, Miezin FM, Petersen SE (2002): Functional neuroanatomical differences between adults and school-age children in the processing of single words. Science 296:1476-1479.
79. Small DM, Gitelman DR, Gregory MD, Nobre AC, Parrish TB, Mesulam MM (2003): The posterior cingulate and medial prefrontal cortex mediate the anticipatory allocation of spatial attention. Neuroimage 18:633-641.
80. Sowell ER, Thompson PM, Holmes CJ, Jernigan TL, Toga AW (1999a): In vivo evidence for post-adolescent brain maturation in frontal and striatal regions. Nat Neurosci 2:859-861.
81. Sowell ER, Thompson PM, Holmes CJ, Barth R, Jernigan TL, Toga AW(1999b): Localizing age-related changes in brain structure between childhood and adolescence using statistical parametric mapping. Neuroimage 9:587-597.
82. Sowell ER, Thompson PM, Toga AW(2004): Mapping changes in the human cortex throughout the span of life. Neuroscientist 10:372-392.
83. Talairach J, Tournoux P (1988): Co-planar Stereotaxic Atlas of the Brain. New York: Thieme.
84. Tamm L, Menon V, Reiss AL (2002): Maturation of brain function associated with response inhibition. J Am Acad Child Adolesc Psychiatry 41:1231-1238.
85. Thomas KM, Hunt RH, Vizueta N, Sommer T, Durston S, Yang YH, Worden MS (2004): Evidence of developmental differences in implicit sequence learning: An fMRI study of children and adults. J Cogn Neurosci 16:1339-1351.
86. Ullsperger M, von Cramon DY (2001): Subprocesses of performance monitoring: A dissociation of error processing and response competition revealed by event-related fMRI and ERPs. Neuroimage 14:1387-1401.
87. Ullsperger M, von Cramon DY (2004a): Decision making, performance and outcome monitoring in frontal cortical areas. Nat Neurosci 7:1173-1174.
88. Ullsperger M, von Cramon DY (2004b): Neuroimaging of performance monitoring: Error detection and beyond. Cortex 40:593-604.
89. Vink M, Kahn RS, Raemakers M, van den Heuvel M, Boersma M, Ramsey NF (2005): Function of striatum beyond inhibition and execution of motor responses. Hum Brain Mapp 25:336-344.
90. Williams BR, Ponesse JS, Schachar RJ, Logan GD, Tannock R (1999): Development of inhibitory control across the life span. Dev Psychol 35:205-213.