Cortical neurodynamics of inhibitory control

Journal of Neuroscience

Volumn 34, Issue 29, 2014, Pages 9551-9561

  Hwang, Kai ^a,b   Ghuman, Avniel S ^a,b   Manoach, Dara S ^c   Jones, Stephanie R ^a,c,d   Luna, Beatriz ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d BROWN UNIVERSITY   (United States)

Author keywords

Antisaccade; Inhibitory control; Neural oscillations; Prefrontal cortex

Indexed keywords

ANTISACCADE; INHIBITORY CONTROL; NEURAL OSCILLATIONS; PREFRONTAL CORTEX;

ADULT; ANALYSIS OF VARIANCE; BRAIN MAPPING; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; INHIBITION (PSYCHOLOGY); MAGNETOENCEPHALOGRAPHY; MALE; NONLINEAR DYNAMICS; PREFRONTAL CORTEX; REACTION TIME; SACCADES; SPECTRUM ANALYSIS; VISUAL FIELDS; YOUNG ADULT;

EID: 84904295473     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4889-13.2014     Document Type: Article

References (92)

1. Akaishi R, Morishima Y, Rajeswaren VP, Aoki S, Sakai K (2010) Stimulation of the frontal eye field reveals persistent effective connectivity after controlled behavior. J Neurosci 30:4295-4305. CrossRef Medline
2. Alexander GE, De Long MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381. CrossRef Medline
3. Anderson JC, Kennedy H, Martin KA (2011) Pathways of attention: synaptic relationships of frontal eye field to V4, lateral intraparietal cortex, and area 46 in macaque monkey. J Neurosci 31:10872-10881. CrossRef Medline
4. Aron AR (2011) From reactive to proactive and selective control: developing a richer model for stopping inappropriate responses. Biol Psychiatry 69:e55-68. CrossRef Medline
5. 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
6. 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
7. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170-177. CrossRef Medline
8. 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
9. Badre D, D'Esposito M (2009) Is the rostro-caudal axis of the frontal lobe hierarchical? Nat Rev Neurosci 10:659-669. CrossRef Medline
10. Banerjee S, Snyder AC, Molholm S, Foxe JJ (2011) Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: supramodal or sensory-specific control mechanisms? J Neurosci 31:9923-9932. CrossRef Medline
11. Belyusar D, Snyder AC, Frey HP, Harwood MR, Wallman J, Foxe JJ (2013) Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task. Neuroimage 65: 395-407. CrossRef Medline
12. Berman RA, Colby CL, Genovese CR, Voyvodic JT, Luna B, Thulborn KR, Sweeney JA (1999) Cortical networks subserving pursuit and saccadic eye movements in humans: an f MRI study. Hum Brain Mapp 8:209-225. CrossRef Medline
13. Bollimunta A, Mo J, Schroeder CE, Ding M (2011) Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J Neurosci 31:4935-4943. CrossRef Medline
14. Brown MR, Vilis T, Everling S (2007) Frontoparietal activation with preparation for antisaccades. J Neurophysiol 98 1751-1762.
15. Buschman TJ, Miller EK (2007) Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 315: 1860-1862. CrossRef Medline
16. Buschman TJ, Denovellis EL, Diogo C, Bullock D, Miller EK (2012) Synchronous oscillatory neural ensembles for rules in the prefrontal cortex. Neuron 76:838-846. CrossRef Medline
17. Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14:506-515. CrossRef Medline
18. Chikazoe J, Konishi S, Asari T, Jimura K, Miyashita Y (2007) Activation of right inferior frontal gyrus during response inhibition across response modalities. J Cogn Neurosci 19:69-80. CrossRef Medline
19. Cohen MX (2011) It's about time. Front Hum Neurosci 5:2. CrossRef Medline
20. Connolly JD, Goodale MA, Menon RS, Munoz DP (2002) Human f MRI evidence for the neural correlates of preparatory set. Nat Neurosci 5:1345-1352. CrossRef Medline
21. Courtemanche R, Fujii N, Graybiel AM (2003) Synchronous, focally modulated beta-band oscillations characterize local field potential activity in the striatum of awake behaving monkeys. J Neurosci 23:11741-11752. Medline
22. Criaud M, Boulinguez P (2013) Have we been asking the right questions when assessing response inhibition in go/no-go tasks with f MRI? A metaanalysis and critical review. Neurosci Biobehav Rev 37:11-23. CrossRef Medline
23. Curtis CE (2011) Testing animal models of human oculomotor control with neuroimaging. In: The Oxford handbook of eye movements (Liversedge SP, Gilchrist ID, Everling S, eds), pp 383-398. New York: Oxford UP.
24. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 9:179-194. CrossRef Medline
25. Dale AM, Liu AK, Fischl BR, Buckner RL, Belliveau JW, Lewine JD, Halgren E (2000) Dynamic statistical parametric mapping: combining f MRI and MEG for high-resolution imaging of cortical activity. Neuron 26:55-67. CrossRef Medline
26. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9-21. CrossRef Medline
27. DeSouza J, Menon RS, Everling S (2003) Preparatory set associated with pro-saccades and anti-saccades in humans investigated with event-related f MRI. J Neurophysiol 89:1016-1023. Medline
28. Destrieux C, Fischl B, Dale A, Halgren E (2010) Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 53:1-15. CrossRef Medline
29. Ding M, Chen Y, Bressler SL (2006) Granger causality: basic theory and application to neuroscience. In: Handbook of time series analysis: recent theoretical developments and applications (Schelter B, Winterhalder M, Timmer J, eds), p 437. Weinheim, Germany: Wiley-VCH.
30. Donner TH, Siegel M (2011) A framework for local cortical oscillation patterns. Trends Cogn Sci 15:191-199. CrossRef Medline
31. Everling S, Munoz DP (2000) Neuronal correlates for preparatory set associated with pro-saccades and anti-saccades in the primate frontal eye field. J Neurosci 20:387-400. Medline
32. Everling S, Dorris MC, Klein RM, Munoz DP (1999) Role of primate superior colliculus in preparation and execution of anti-saccades and prosaccades. J Neurosci 19:2740-2754. Medline
33. Fischl B, Sereno MI, Dale AM (1999) Cortical surface-based analysis. II. Inflation, flattening, and a surface-based coordinate system. Neuroimage 9:195-207. CrossRef Medline
34. Ford KA, Goltz HC, Brown MR, Everling S (2005) Neural processes associated with antisaccade task performance investigated with event-related FMRI. J Neurophysiol 94:429-440. CrossRef Medline
35. Foxe JJ, Simpson GV, Ahlfors SP (1998) Parieto-occipital approximately 10 Hz activity reflects anticipatory state of visual attention mechanisms. Neuroreport 9:3929-3933. CrossRef Medline
36. Gentet LJ, Kremer Y, Taniguchi H, Huang ZJ, Staiger JF, Petersen CC (2012) Unique functional properties of somatostatin-expressing GABAergic neurons in mouse barrel cortex. Nat Neurosci 15:607-612. CrossRef Medline
37. Ghuman AS, McDaniel JR, Martin A (2011) A wavelet-based method for measuring the oscillatory dynamics of resting-state functional connectivity in MEG. Neuroimage 56:69-77. CrossRef Medline
38. Gottlieb J, Goldberg ME (1999) Activity of neurons in the lateral intraparietal area of the monkey during an antisaccade task. Nat Neurosci 2:906-912. CrossRef Medline
39. Grosbras MH, Lobel E, Van de Moortele PF, Le Bihan D, Berthoz A (1999) An anatomical landmark for the supplementary eye fields in human revealed with functional magnetic resonance imaging. Cereb Cortex 9:705-711. CrossRef Medline
40. Gross J, Baillet S, Barnes GR, Henson RN, Hillebrand A, Jensen O, Jerbi K, Litvak V, Maess B, Oostenveld R, Parkkonen L, Taylor JR, van Wassenhove V, Wibral M, Schoffelen JM (2013) Good practice for conducting and reporting MEG research. Neuroimage 65:349-363. CrossRef Medline
41. Haegens S, Nácher V, Luna R, Romo R, Jensen O (2011) Alpha-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc Natl Acad Sci U S A 108:19377-19382. CrossRef Medline
42. Hallett PE (1978) Primary and secondary saccades to goals defined by instructions. Vision Res 18:1279-1296. CrossRef Medline
43. Hamalainen MS (2010) MNE software user's guide. Charlestown, MA: Massachusetts General Hospital.
44. Hämäläinen MS, Sarvas J (1989) Realistic conductivity geometry model of the human head for interpretation of neuromagnetic data. IEEE Trans Biomed Eng 36:165-171. CrossRef Medline
45. Hamalainen MS, Lin FH, Mosher JC (2010) Anatomically and functionally constrained minimum-norm estimates. In: MEG: an introduction to methods (Hansen PC, Kringelbach ML, Salmelin R, eds), pp 186-215. New York: Oxford UP.
46. Hamm JP, Dyckman KA, McDowell JE, Clementz BA (2012) Pre-cue fronto-occipital alpha phase and distributed cortical oscillations predict failures of cognitive control. J Neurosci 32:7034-7041. CrossRef Medline
47. Hikosaka O, Takikawa Y, Kawagoe R (2000) Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol Rev 80:953-978. Medline
48. Hodgson T, Chamberlain M, Parris B, James M, Gutowski N, Husain M, Kennard C (2007) The role of the ventrolateral frontal cortex in inhibitory oculomotor control. Brain 130:1525-1537. CrossRef Medline
49. Hughes SW, Crunelli V (2005) Thalamic mechanisms of EEG alpha rhythms and their pathological implications. Neuroscientist 11:357-372. CrossRef Medline
50. Hwang K, Velanova K, Luna B (2010) Strengthening of top-down frontal cognitive control networks underlying the development of inhibitory control: a functional magnetic resonance imaging effective connectivity study. J Neurosci 30:15535-15545. CrossRef Medline
51. Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186. CrossRef Medline
52. Johnston K, Everling S (2011) Frontal cortex and saccadic control. In: The Oxford handbook of eye movements (Liversedge SP, Gilchrist ID, Everling S, eds), pp 279-302. New York: Oxford UP.
53. Johnston K, Koval MJ, Lomber SG, Everling S (2014) Macaque dorsolateral prefrontal cortex does not suppress saccade-related activity in the superior colliculus. Cereb Cortex 24:1373-1388. CrossRef Medline
54. Jones EG (2001) The thalamic matrix and thalamocortical synchrony. Trends Neurosci 24:595-601. CrossRef Medline
55. Jones SR, Pritchett DL, Sikora MA, Stufflebeam SM, Hämäläinen M, Moore CI (2009) Quantitative analysis and biophysically realistic neural modeling of the MEG mu rhythm: rhythmogenesis and modulation of sensory-evoked responses. J Neurophysiol 102:3554-3572. CrossRef Medline
56. Jones SR, Kerr CE, Wan Q, Pritchett DL, Hämäläinen M, Moore CI (2010) Cued spatial attention drives functionally relevant modulation of the mu rhythm in primary somatosensory cortex. J Neurosci 30:13760-13765. CrossRef Medline
57. Kelly SP, Foxe JJ, Newman G, Edelman JA (2010) Prepare for conflict: EEG correlates of the anticipation of target competition during overt and covert shifts of visual attention. Eur J Neurosci 31:1690-1700. CrossRef Medline
58. Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 53:63-88. CrossRef Medline
59. Koval MJ, Lomber SG, Everling S (2011) Prefrontal cortex deactivation in macaques alters activity in the superior colliculus and impairs voluntary control of saccades. J Neurosci 31:8659-8668. CrossRef Medline
60. Lee AK, Hämäläinen MS, Dyckman KA, Barton JJ, Manoach DS (2011) Saccadic preparation in the frontal eye field is modulated by distinct trial history effects as revealed by magnetoencephalography. Cereb Cortex 21: 245-253. CrossRef Medline
61. 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
62. Luna B, Thulborn KR, Strojwas MH, McCurtain BJ, Berman RA, Genovese CR, Sweeney JA (1998) Dorsal cortical regions subserving visuallyguided saccades in humans: an f MRI study. Cereb Cortex 8:40-47. CrossRef Medline
63. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG-and MEG-data. J Neurosci Methods 164:177-190. CrossRef Medline
64. Mazaheri A, Nieuwenhuis IL, van Dijk H, Jensen O (2009) Prestimulus alpha and mu activity predicts failure to inhibit motor responses. Hum Brain Mapp 30:1791-1800. CrossRef Medline
65. Menon V, Adleman NE, White CD, Glover GH, Reiss AL (2001) Errorrelated brain activation during a Go/No Go response inhibition task. Hum Brain Mapp 12:131-143. CrossRef Medline
66. Moon SY, Barton JJ, Mikulski S, Polli FE, Cain MS, Vangel M, Hämäläinen MS, Manoach DS (2007) Where left becomes right: a magnetoencephalographic study of sensorimotor transformation for antisaccades. Neuroimage 36:1313-1323. CrossRef Medline
67. Munakata Y, Herd SA, Chatham CH, Depue BE, Banich MT, O'Reilly RC (2011) A unified framework for inhibitory control. Trends Cogn Sci 15: 453-459. CrossRef Medline
68. Munoz DP, Everling S (2004) Look away: the anti-saccade task and the voluntary control of eye movement. Nat Rev Neurosci 5:218-228. CrossRef Medline
69. Nambu A, Tokuno H, Takada M (2002) Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res 43:111-117. CrossRef Medline
70. Nenonen J, Nurminen J, Kičić D, Bikmullina R, Lioumis P, Jousmäki V, Taulu S, Parkkonen L, Putaala M, Kähkönen S (2012) Validation of head movement correction and spatiotemporal signal space separation in magnetoencephalography. Clin Neurophysiol 123:2180-2191. CrossRef Medline
71. Nieuwenhuis IL, Takashima A, Oostenveld R, McNaughton BL, Fernández G, Jensen O (2012) The neocortical network representing associative memory reorganizes with time in a process engaging the anterior temporal lobe. Cereb Cortex 22:2622-2633. CrossRef Medline
72. Nyffeler T, Müri R, Bucher-Ottiger Y, Pierrot-Deseilligny C, Gaymard B, Rivaud-Pechoux S (2007) Inhibitory control of the human dorsolateral prefrontal cortex during the anti-saccade paradigm-a transcranial magnetic stimulation study. Eur J Neurosci 26:1381-1385. CrossRef Medline
73. Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) Field Trip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. CrossRef Medline
74. Romei V, Brodbeck V, Michel C, Amedi A, Pascual-Leone A, Thut G (2008) Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cereb Cortex 18:2010-2018. CrossRef Medline
75. 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. CrossRef Medline
76. Schiller PH, Sandell JH, Maunsell JH (1987) The effect of frontal eye field and superior colliculus lesions on saccadic latencies in the rhesus monkey. J Neurophysiol 57:1033-1049. Medline
77. Schoffelen JM, Gross J (2009) Source connectivity analysis with MEG and EEG. Hum Brain Mapp 30:1857-1865. CrossRef Medline
78. Selemon LD, Goldman-Rakic PS (1988) Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior. J Neurosci 8:4049-4068. Medline
79. Seth AK (2010) A MATLAB toolbox for Granger causal connectivity analysis. J Neurosci Methods 186:262-273. CrossRef Medline
80. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of largescale neuronal interactions. Nat Rev Neurosci 13:121-134. CrossRef Medline
81. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, Di Sano M, Aron AR (2009) Intracranial EEG reveals a time-and frequencyspecific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. J Neurosci 29:12675-12685. CrossRef Medline
82. Tallon-Baudry C, Bertrand O, Delpuech C, Permier J (1997) Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. J Neurosci 17:722-734. Medline
83. Tan Z, Hu H, Huang ZJ, Agmon A (2008) Robust but delayed thalamocortical activation of dendritic-targeting inhibitory interneurons. Proc Natl Acad Sci U S A 105:2187-2192. CrossRef Medline
84. Taulu S, Hari R (2009) Removal of magnetoencephalographic artifacts with temporal signal-space separation: demonstration with single-trial auditory-evoked responses. Hum Brain Mapp 30:1524-1534. CrossRef Medline
85. Taulu S, Kajola M, Simola J (2004) Suppression of interference and artifacts by the Signal Space Separation Method. Brain Topogr 16:269-275. Medline
86. Van Der Werf J, Jensen O, Fries P, Medendorp WP (2008) Gamma-band activity in human posterior parietal cortex encodes the motor goal during delayed prosaccades and antisaccades. J Neurosci 28:8397-8405. CrossRef Medline
87. van Dijk H, Schoffelen JM, Oostenveld R, Jensen O (2008) Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 28:1816-1823. CrossRef Medline
88. Vierling-Claassen D, Cardin JA, Moore CI, Jones SR (2010) Computational modeling of distinct neocortical oscillations driven by cell-type selective optogenetic drive: separable resonant circuits controlled by lowthreshold spiking and fast-spiking interneurons. Front Hum Neurosci 4:198. CrossRef Medline
89. Wang XJ (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195-1268. CrossRef Medline
90. Wehner DT, Hämäläinen M, Mody M, Ahlfors SP (2008) Head movements of children in MEG: quantification, effects on source estimation, and compensation. Neuroimage 40:541-550. CrossRef Medline
91. Worden MS, Foxe JJ, Wang N, Simpson GV (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-band electroencephalography increases over occipital cortex. J Neurosci 20:RC63. Medline
92. Zhang M, Barash S (2000) Neuronal switching of sensorimotor transformations for antisaccades. Nature 408:971-975. CrossRef Medline