Reduced cognitive control of response inhibition by the anterior cingulate cortex in autism spectrum disorders

NeuroImage

Volumn 52, Issue 1, 2010, Pages 336-347

  Agam, Yigal ^a,b   Joseph, Robert M ^c   Barton, Jason J S ^d   Manoach, Dara S ^a,b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; AUTISM; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; CINGULATE GYRUS; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE SEVERITY; DORSAL ANTERIOR CINGULATE CORTEX; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; MALE; MOTOR CONTROL; PRIORITY JOURNAL; SACCADIC EYE MOVEMENT; VISUAL FIELD; VISUAL STIMULATION; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COGNITION; EXECUTIVE FUNCTION; FRONTAL LOBE; INFANT; INHIBITION (PSYCHOLOGY); NERVE TRACT; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; OCULOGRAPHY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOMOTOR PERFORMANCE; TIME;

ADULT; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COGNITION; EXECUTIVE FUNCTION; EYE MOVEMENT MEASUREMENTS; FEMALE; FRONTAL LOBE; GYRUS CINGULI; HUMANS; INFANT; INHIBITION (PSYCHOLOGY); MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; NEUROPSYCHOLOGICAL TESTS; PSYCHOMOTOR PERFORMANCE; SACCADES; TIME FACTORS;

EID: 77953288657     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.04.010     Document Type: Article

References (111)

1. Ashwin C., Baron-Cohen S., Wheelwright S., O'Riordan M., Bullmore E.T. Differential activation of the amygdala and the "social brain" during fearful face-processing in Asperger syndrome. Neuropsychologia 2007, 45:2-14.
2. Barnea-Goraly N., Kwon H., Menon V., Eliez S., Lotspeich L., Reiss A.L. White matter structure in autism: preliminary evidence from diffusion tensor imaging. Biol. Psychiatry 2004, 55:323-326.
3. Bishop D.V., Norbury C.F. Executive functions in children with communication impairments, in relation to autistic symptomatology. 2: response inhibition. Autism 2005, 9:29-43.
4. Biswal B., Yetkin F.Z., Haughton V.M., Hyde J.S. Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn. Reson. Med. 1995, 34:537-541.
5. Blair J.R., Spreen O. Predicting premorbid IQ: a revision of the National Adult Reading Test. Clin. Neuropsychol. 1989, 3:129-136.
6. Brown M.R., Goltz H.C., Vilis T., Ford K.A., Everling S. Inhibition and generation of saccades: rapid event-related fMRI of prosaccades, antisaccades, and nogo trials. Neuroimage 2006, 33:644-659.
7. Buckner R.L., Goodman J., Burock M., Rotte M., Koutstaal W., Schacter D., et al. Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 1998, 20:285-296.
8. Buckner R.L., Andrews-Hanna J.R., Schacter D.L. The brain's default network: anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 2008, 1124:1-38.
9. Burock M.A., Dale A.M. Estimation and detection of event-related fMRI signals with temporally correlated noise: a statistically efficient and unbiased approach. Hum. Brain Mapp. 2000, 11:249-260.
10. Bush G., Whalen P.J., Rosen B.R., Jenike M.A., McInerney S.C., Rauch S.L. The counting stroop: an interference task specialized for functional neuroimaging-validation study with functional MRI. Hum. Brain Mapp. 1998, 6:270-282.
11. Bush G., Luu P., Posner M.I. Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn. Sci. 2000, 4:215-222.
12. Cherkassky V.L., Kana R.K., Keller T.A., Just M.A. Functional connectivity in a baseline resting-state network in autism. Neuroreport 2006, 17:1687-1690.
13. Collins D.L., Neelin P., Peters T.M., Evans A.C. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994, 18:192-205.
14. Connolly J.D., Goodale M.A., Menon R.S., Munoz D.P. Human fMRI evidence for the neural correlates of preparatory set. Nat. Neurosci. 2002, 5:1345-1352.
15. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
16. Cox R.W., Jesmanowicz A. Real-time 3D image registration for functional MRI. Magn. Reson. Med. 1999, 42:1014-1018.
17. Dale A.M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 1999, 8:109-140.
18. Dale A.M., Fischl B., Sereno M.I. Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999, 9:179-194.
19. DeSouza J.F., Menon R.S., Everling S. Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related FMRI. J. Neurophysiol. 2003, 89:1016-1023.
20. Devinsky O., Morrell M.J., Vogt B.A. Contributions of anterior cingulate cortex to behaviour. Brain 1995, 118(Pt 1):279-306.
21. Dichter G.S., Belger A. Social stimuli interfere with cognitive control in autism. Neuroimage 2007, 35:1219-1230.
22. Doricchi F., Perani D., Inoccia C., Grassi F., Cappa S.F., Bettinardi V., et al. Neural control of fast-regular saccades and antisaccades: an investigation using positron emission tomography. Exp. Brain Res. 1997, 116:50-62.
23. Everling S., Munoz D.P. Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J. Neurosci. 2000, 20:387-400.
24. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured Clinical Interview for DSM-IV-TR Axis I Disorders, Research Version 2002, Biometrics Research, New York State Psychiatric Institute, New York. Nonpatient Edition.
25. Fischer B., Breitmeyer B. Mechanisms of visual attention revealed by saccadic eye movements. Neuropsychologia 1987, 25:73-83.
26. Fischl B., Sereno M.I., Dale A.M. Cortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 1999, 9:195-207.
27. Fischl B., Sereno M.I., Tootell R.B.H., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum. Brain Mapp. 1999, 8:272-284.
28. Fischl B., van der Kouwe A., Destrieux C., Halgren E., Segonne F., Salat D.H., et al. Automatically parcellating the human cerebral cortex. Cereb. Cortex 2004, 14:11-22.
29. Ford K.A., Goltz H.C., Brown M.R., Everling S. Neural processes associated with antisaccade task performance investigated with event-related FMRI. J. Neurophysiol. 2005, 94:429-440.
30. Ford K.A., Gati J.S., Menon R.S., Everling S. BOLD fMRI activation for anti-saccades in nonhuman primates. Neuroimage 2009, 45:470-476.
31. Fox M.D., Snyder A.Z., Vincent J.L., Corbetta M., Van Essen D.C., Raichle M.E. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:9673-9678.
32. Gaymard B., Rivaud S., Cassarini J.F., Dubard T., Rancurel G., Agid Y., Pierrot-Deseilligny C. Effects of anterior cingulate cortex lesions on ocular saccades in humans. Exp. Brain Res. 1998, 120:173-183.
33. Geschwind D.H. Advances in autism. Annu. Rev. Med. 2009, 60:367-380.
34. Geurts H.M., Verte S., Oosterlaan J., Roeyers H., Sergeant J.A. How specific are executive functioning deficits in attention deficit hyperactivity disorder and autism?. J. Child Psychol. Psychiatry 2004, 45:836-854.
35. Gitelman D.R., Nobre A.C., Parrish T.B., LaBar K.S., Kim Y.H., Meyer J.R., Mesulam M. A large-scale distributed network for covert spatial attention: further anatomical delineation based on stringent behavioural and cognitive controls. Brain 1999, 122:1093-1106.
36. Goldberg M.C., Lasker A.G., Zee D.S., Garth E., Tien A., Landa R.J. Deficits in the initiation of eye movements in the absence of a visual target in adolescents with high functioning autism. Neuropsychologia 2002, 40:2039-2049.
37. Goldberg M.C., Mostofsky S.H., Cutting L.E., Mahone E.M., Astor B.C., Denckla M.B., Landa R.J. Subtle executive impairment in children with autism and children with ADHD. J. Autism Dev. Disord. 2005, 35:279-293.
38. Gomot M., Bernard F.A., Davis M.H., Belmonte M.K., Ashwin C., Bullmore E.T., Baron-Cohen S. Change detection in children with autism: an auditory event-related fMRI study. Neuroimage 2006, 29:475-484.
39. Hall G.B., Szechtman H., Nahmias C. Enhanced salience and emotion recognition in Autism: a PET study. Am. J. Psychiatry 2003, 160:1439-1441.
40. Hallett P.E. Primary and secondary saccades to goals defined by instructions. Vision Res. 1978, 18:1279-1296.
41. Happe F., Ronald A., Plomin R. Time to give up on a single explanation for autism. Nat. Neurosci. 2006, 9:1218-1220.
42. Haznedar M.M., Buchsbaum M.S., Metzger M., Solimando A., Spiegel-Cohen J., Hollander E. Anterior cingulate gyrus volume and glucose metabolism in autistic disorder. Am. J. Psychiatry 1997, 154:1047-1050.
43. Haznedar M.M., Buchsbaum M.S., Wei T.C., Hof P.R., Cartwright C., Bienstock C.A., Hollander E. Limbic circuitry in patients with autism spectrum disorders studied with positron emission tomography and magnetic resonance imaging. Am. J. Psychiatry 2000, 157:1994-2001.
44. Henderson H., Schwartz C., Mundy P., Burnette C., Sutton S., Zahka N., Pradella A. Response monitoring, the error-related negativity, and differences in social behavior in autism. Brain Cogn. 2006, 61:96-109.
45. Hill E.L. Executive dysfunction in autism. Trends Cogn. Sci. 2004, 8:26-32.
46. Hollingshead A.B. Two factor index of social position 1965, Yale University Press, New Haven, Conn.
47. Huerta M.F., Krubitzer L.A., Kaas J.H. Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys. II. Cortical connections. J. Comp. Neurol. 1987, 265:332-361.
48. Hunt A.R., Kingstone A. Covert and overt voluntary attention: linked or independent?. Brain Res. Cogn. Brain Res. 2003, 18:102-105.
49. Johnston K., Levin H.M., Koval M.J., Everling S. Top-down control-signal dynamics in anterior cingulate and prefrontal cortex neurons following task switching. Neuron 2007, 53:453-462.
50. Just M.A., Cherkassky V.L., Keller T.A., Minshew N.J. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain 2004, 127:1811-1821.
51. Kana R.K., Keller T.A., Minshew N.J., Just M.A. Inhibitory control in high-functioning autism: decreased activation and underconnectivity in inhibition networks. Biol. Psychiatry 2007, 62:198-206.
52. Kennedy D.P., Courchesne E. The intrinsic functional organization of the brain is altered in autism. Neuroimage 2008, 39:1877-1885.
53. Kennedy D.P., Redcay E., Courchesne E. Failing to deactivate: resting functional abnormalities in autism. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:8275-8280.
54. Klein C., Foerster F. Development of prosaccade and antisaccade task performance in participants aged 6 to 26years. Psychophysiology 2001, 38:179-189.
55. Klein R., McCormick P. Covert visual orienting: hemifield-activation can be mimicked by zoom lens and midlocation placement strategies. Acta Psychol. (Amst.) 1989, 70:235-250.
56. Kleinhans N., Akshoomoff N., Delis D.C. Executive functions in autism and Asperger's disorder: flexibility, fluency, and inhibition. Dev. Neuropsychol. 2005, 27:379-401.
57. Kleinhans N.M., Richards T., Sterling L., Stegbauer K.C., Mahurin R., Johnson L.C., et al. Abnormal functional connectivity in autism spectrum disorders during face processing. Brain 2008, 131:1000-1012.
58. Koski L., Paus T. Functional connectivity of the anterior cingulate cortex within the human frontal lobe: a brain-mapping meta-analysis. Exp. Brain Res. 2000, 133:55-65.
59. Koyama M., Hasegawa I., Osada T., Adachi Y., Nakahara K., Miyashita Y. Functional magnetic resonance imaging of macaque monkeys performing visually guided saccade tasks: comparison of cortical eye fields with humans. Neuron 2004, 41:795-807.
60. London E. The role of the neurobiologist in redefining the diagnosis of autism. Brain Pathol. 2007, 17:408-411.
61. Lopez B.R., Lincoln A.J., Ozonoff S., Lai Z. Examining the relationship between executive functions and restricted, repetitive symptoms of autistic disorder. J. Autism Dev. Disord. 2005, 35:445-460.
62. Lord C., Rutter M., DiLavore P.C., Risi S. Autism Diagnostic Observation Schedule-WPS (ADOS-WPS) 1999, Western Psychological Services, Los Angeles, CA.
63. Luna B., Doll S.K., Hegedus S.J., Minshew N.J., Sweeney J.A. Maturation of executive function in autism. Biol. Psychiatry 2007, 61:474-481.
64. Mahone E.M., Powell S.K., Loftis C.W., Goldberg M.C., Denckla M.B., Mostofsky S.H. Motor persistence and inhibition in autism and ADHD. J. Int. Neuropsychol. Soc. 2006, 12:622-631.
65. Manoach D.S., Weintraub S., Daffner K.R., Scinto L.F. Deficient antisaccades in the social-emotional processing disorder. Neuroreport 1997, 8:901-905.
66. Manoach D.S., Lindgren K.A., Cherkasova M.V., Goff D.C., Halpern E.F., Intriligator J., Barton J.J.S. Schizophrenic subjects show deficient inhibition but intact task-switching on saccadic tasks. Biol. Psychiatry 2002, 51:816-826.
67. Manoach D.S., Lindgren K.A., Barton J.J. Deficient saccadic inhibition in Asperger's disorder and the social-emotional processing disorder. J. Neurol. Neurosurg. Psychiatry 2004, 75:1719-1726.
68. Manoach D.S., Thakkar K.N., Cain M.S., Polli F.E., Edelman J.A., Fischl B., Barton J.J. Neural activity is modulated by trial history: a functional magnetic resonance imaging study of the effects of a previous antisaccade. J. Neurosci. 2007, 27:1791-1798.
69. Margulies D.S., Kelly A.M., Uddin L.Q., Biswal B.B., Castellanos F.X., Milham M.P. Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 2007, 37:579-588.
70. Matsuda T., Matsuura M., Ohkubo T., Ohkubo H., Matsushima E., Inoue K., et al. Functional MRI mapping of brain activation during visually guided saccades and antisaccades: cortical and subcortical networks. Psychiatry Res. 2004, 131:147-155.
71. Mesulam M.-M. A cortical network for directed attention and unilateral neglect. Ann. Neurol. 1981, 10:309-325.
72. Mesulam M.M. Large-scale neurocognitive networks and distributed processing for attention, language, and memory. Ann. Neurol. 1990, 28:597-613.
73. Miezin F.M., Maccotta L., Ollinger J.M., Petersen S.E., Buckner R.L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure, and the possibility of ordering brain activity based on relative timing. Neuroimage 2000, 11:735-759.
74. Milea D., Lehericy S., Rivaud-Pechoux S., Duffau H., Lobel E., Capelle L., et al. Antisaccade deficit after anterior cingulate cortex resection. Neuroreport 2003, 14:283-287.
75. Miller E.K., Cohen J.D. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 2001, 24:167-202.
76. Minshew N.J., Luna B., Sweeney J.A. Oculomotor evidence for neocortical systems but not cerebellar dysfunction in autism. Neurology 1999, 52:917-922.
77. Mitz A.R., Godschalk M. Eye-movement representation in the frontal lobe of rhesus monkeys. Neurosci. Lett. 1989, 106:157-162.
78. Moore T., Armstrong K.M., Fallah M. Visuomotor origins of covert spatial attention. Neuron 2003, 40:671-683.
79. Morecraft R.J., Geula C., Mesulam M.M. Architecture of connectivity within a cingulo-fronto-parietal neurocognitive network for directed attention. Arch. Neurol. 1993, 50:279-284.
80. Mosconi M.W., Kay M., D'Cruz A.M., Seidenfeld A., Guter S., Stanford L.D., Sweeney J.A. Impaired inhibitory control is associated with higher-order repetitive behaviors in autism spectrum disorders. Psychol. Med. 2009, 1-8.
81. Mundy P. Annotation: the neural basis of social impairments in autism: the role of the dorsal medial-frontal cortex and anterior cingulate system. J. Child Psychol. Psychiatry 2003, 44:793-809.
82. Mundy P., Sullivan L., Mastergeorge A.M. A parallel and distributed-processing model of joint attention, social cognition and autism. Autism Res. 2009, 2:2-21.
83. Munoz D.P., Everling S. Look away: the anti-saccade task and the voluntary control of eye movement. Nat. Rev. Neurosci. 2004, 5:218-228.
84. O'Driscoll G.A., Alpert N.M., Matthysse S.W., Levy D.L., Rauch S.L., Holzman P.S. Functional neuroanatomy of antisaccade eye movements investigated with positron emission tomography. Proc. Natl. Acad. Sci. U. S. A. 1995, 92:925-929.
85. Ohnishi T., Matsuda H., Hashimoto T., Kunihiro T., Nishikawa M., Uema T., Sasaki M. Abnormal regional cerebral blood flow in childhood autism. Brain 2000, 123(Pt 9):1838-1844.
86. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
87. Ozonoff S., Strayer D.L. Inhibitory function in nonretarded children with autism. J. Autism Dev. Disord. 1997, 27:59-77.
88. Pandya D.N., Van Hoesen G.W., Mesulam M.M. Efferent connections of the cingulate gyrus in the rhesus monkey. Exp. Brain Res. 1981, 42:319-330.
89. Paus T. Location and function of the human frontal eye-field: a selective review. Neuropsychologia 1996, 34:475-483.
90. Paus T., Petrides M., Evans A.C., Meyer E. Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J. Neurophysiol. 1993, 70:453-469.
91. Phillips M.L., Drevets W.C., Rauch S.L., Lane R. Neurobiology of emotion perception I: the neural basis of normal emotion perception. Biol. Psychiatry 2003, 54:504-514.
92. Pierrot-Deseilligny C., Rivaud S., Gaymard B., Muri R., Vermersch A.I. Cortical control of saccades. Ann. Neurol. 1995, 37:557-567.
93. Pierrot-Deseilligny C., Milea D., Muri R.M. Eye movement control by the cerebral cortex. Curr. Opin. Neurol. 2004, 17:17-25.
94. Polli F.E., Barton J.J., Cain M.S., Thakkar K.N., Rauch S.L., Manoach D.S. Rostral and dorsal anterior cingulate cortex make dissociable contributions during antisaccade error commission. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:15700-15705.
95. Raymaekers R., van der Meere J., Roeyers H. Event-rate manipulation and its effect on arousal modulation and response inhibition in adults with high functioning autism. J. Clin. Exp. Neuropsychol. 2004, 26:74-82.
96. Rommelse N.N., Van der Stigchel S., Sergeant J.A. A review on eye movement studies in childhood and adolescent psychiatry. Brain Cogn. 2008, 68:391-414.
97. Rutter M., Le Couteur A., Lord C. Autism Diagnostic Interview-Revised 2003, Western Psychological Services, Los Angeles, CA.
98. Schmitz N., Rubia K., Daly E., Smith A., Williams S., Murphy D.G. Neural correlates of executive function in autistic spectrum disorders. Biol. Psychiatry 2006, 59:7-16.
99. Shafritz K.M., Dichter G.S., Baranek G.T., Belger A. The neural circuitry mediating shifts in behavioral response and cognitive set in autism. Biol. Psychiatry 2008, 63:974-980.
100. Silk T.J., Rinehart N., Bradshaw J.L., Tonge B., Egan G., O'Boyle M.W., Cunnington R. Visuospatial processing and the function of prefrontal-parietal networks in autism spectrum disorders: a functional MRI study. Am. J. Psychiatry 2006, 163:1440-1443.
101. Solomon M., Ozonoff S.J., Ursu S., Ravizza S., Cummings N., Ly S., Carter C.S. The neural substrates of cognitive control deficits in autism spectrum disorders. Neuropsychologia 2009, 47:2515-2526.
102. South M., Ozonoff S., McMahon W.M. The relationship between executive functioning, central coherence, and repetitive behaviors in the high-functioning autism spectrum. Autism 2007, 11:437-451.
103. Sweeney J.A., Mintun M.A., Kwee S., Wiseman M.B., Brown D.L., Rosenberg D.R., Carl J.R. Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. J. Neurophysiol. 1996, 75:454-468.
104. Thakkar K.N., Polli F.E., Joseph R.M., Tuch D.S., Hadjikhani N., Barton J.J., Manoach D.S. Response monitoring, repetitive behaviour and anterior cingulate abnormalities in autism spectrum disorders (ASD). Brain 2008, 131:2464-2478.
105. Thesen S., Heid O., Mueller E., Schad L.R. Prospective acquisition correction for head motion with image-based tracking for real-time fMRI. Magn. Reson. Med. 2000, 44:457-465.
106. Van Dijk, K.R.A., Hedden, T., Venkataraman, A., Evans, K.C., Lazar, S.W., Buckner, R.L., in press. Functional connectivity MRI: Theory, properties, and optimization. J. Neurophys.
107. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. J. Neurophysiol. 2006, 96:3517-3531.
108. Wang Y., Matsuzaka Y., Shima K., Tanji J. Cingulate cortical cells projecting to monkey frontal eye field and primary motor cortex. Neuroreport 2004, 15:1559-1563.
109. Wechsler D. Wechsler Abbreviated Scale of Intelligence 1999, The Psychological Corporation, San Antonio, TX.
110. Whalen P.J., Bush G., McNally R.J., Wilhelm S., McInerney S.C., Jenike M.A., Rauch S.L. The emotional counting Stroop paradigm: a functional magnetic resonance imaging probe of the anterior cingulate affective division. Biol. Psychiatry 1998, 44:1219-1228.
111. White K., Ashton R. Handedness assessment inventory. Neuropsychologia 1976, 14:261-264.