Attention drives synchronization of alpha and beta rhythms between right inferior frontal and primary sensory neocortex

Journal of Neuroscience

Volumn 35, Issue 5, 2015, Pages 2074-2082

  Sacchet, Matthew D ^a,b   LaPlante, Roan A ^c   Wan, Qian ^d   Pritchett, Dominique L ^e   Lee, Adrian K C ^f   Hämäläinen, Matti ^c   Moore, Christopher I ^g   Kerr, Catherine E ^h   Jones, Stephanie R ^c,g  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b STANFORD UNIVERSITY   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD UNIVERSITY   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f UNIVERSITY OF WASHINGTON   (United States)

^g BROWN UNIVERSITY   (United States)

^h BROWN UNIVERSITY   (United States)

Author keywords

Attention; Inferior frontal cortex; Magnetoencephalography; Primary somatosensory cortex; Somatosensation; Synchrony

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; ASSOCIATION; ATTENTION; BEHAVIOR; BETA RHYTHM; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVOKED MUSCLE RESPONSE; EXPERIMENTAL DESIGN; FEMALE; FUNCTIONAL NEUROIMAGING; HUMAN; MAGNETOENCEPHALOGRAPHY; MALE; NEUROSCIENCE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; RIGHT INFERIOR FRONTAL CORTEX; SENSORY NEOCORTEX; SOMATOSENSORY CORTEX; CORTICAL SYNCHRONIZATION; FRONTAL LOBE; NEOCORTEX; PHYSIOLOGY; SENSORIMOTOR CORTEX; TOUCH;

ADULT; ALPHA RHYTHM; ATTENTION; BETA RHYTHM; CORTICAL SYNCHRONIZATION; CUES; FEMALE; FRONTAL LOBE; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; NEOCORTEX; SENSORIMOTOR CORTEX; TOUCH PERCEPTION;

EID: 84922382789     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1292-14.2015     Document Type: Article

References (81)

1. Amunts K, von Cramon DY (2006) The anatomical segregation of the frontal cortex: what does it mean for function? Cortex 42:525–528. CrossRef Medline
2. Aron AR, Robbins TW, Poldrack RA (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177. CrossRef Medline
3. 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
4. Badre D, Wagner AD (2007) Left ventrolateral prefrontal cortex and the cognitive control of memory. Neuropsychologia 45:2883–2901. CrossRef Medline
5. Baldauf D, Desimone R (2014) Neural mechanisms of object-based attention. Science 334:424. CrossRef Medline
6. Bauer M, Oostenveld R, Peeters M, Fries P (2006) Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces lowfrequency activity in parieto-occipital areas. J Neurosci 26:490–501. CrossRef Medline
7. Bressler SL, Richter CG (2014) Interareal oscillatory synchronization in top-down neocortical processing. Curr Opin Neurobiol 32:62–66. CrossRef Medline
8. Bunge SA (2004) How we use rules to select actions: a review of evidence from cognitive neuroscience. Cogn Affect Behav Neurosci 4:564–579. CrossRef Medline
9. 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
10. 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
11. Chambers CD, Bellgrove MA, Gould IC, English T, Garavan H, McNaught E, Kamke M, Mattingley JB (2007) Dissociable mechanisms of cognitive control in prefrontal and premotor cortex. J Neurophysiol 98:3638–3647. CrossRef Medline
12. 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
13. Dale AM, Sereno MI (1993) Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 5:162–176. CrossRef Medline
14. Dale AM, Fischl B, Sereno MI (1999) Cortical surface-based analysis I. Segmentation and surface reconstruction. Neuroimage 9:179–194. CrossRef Medline
15. Derrfuss J, Vogt VL, Fiebach CJ, von Cramon DY, Tittgemeyer M (2012) Functional organization of the left inferior precentral sulcus: dissociating the inferior frontal eye field and the inferior frontal junction. Neuroimage 59:3829–3837. CrossRef Medline
16. Desikan RS, Ségonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage 31:968–980. CrossRef Medline
17. 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
18. Dockstader C, Cheyne D, Tannock R (2010) Cortical dynamics of selective attention to scholarly events. Neuroimage 49:1777–1785. CrossRef Medline
19. Doesburg SM, Green JJ, McDonald JJ, Ward LM (2009) From local inhibition to long-range integration: a functional dissociation of alpha-band synchronization across cortical scales in visuospatial attention. Brain Res 1303:97–110. CrossRef Medline
20. Donohue SE, Wendelken C, Crone EA, Bunge SA (2005) Retrieving rules for behavior from long-term memory. Neuroimage 26:1140–1149. CrossRef Medline
21. Engel AK, Fries P (2010) Beta band oscillations: signalling the status quo? Curr Opin Neurobiol 20:156–165. CrossRef Medline
22. Ewald A, Marzetti L, Zappasodi F, Meinecke FC, Nolte G (2012) Estimating true brain connectivity from EEG/MEG data invariant to linear and static transformations in sensor space. Neuroimage 60:476–488. CrossRef Medline
23. Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355. CrossRef Medline
24. Fischl B, van der Kouwe A, Destrieux C, Halgren E, Ségonne F, Salat DH, Busa E, Seidman LJ, Goldstein J, Kennedy D, Caviness V, Makris N, Rosen B, Dale AM (2004) Automatically parcellating the human cerebral cortex. Cereb Cortex 14:11–22. CrossRef Medline
25. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480. CrossRef Medline
26. Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224. CrossRef Medline
27. Fritz JB, David SV, Radtke-Schuller S, Yin P, Shamma SA (2010) Adaptive, behaviorally gated, persistent encoding of task-relevant auditory information in ferret frontal cortex. Nat Neurosci 13:1011–1019. CrossRef Medline
28. Gazzaley A, Nobre AC (2012) Top-down modulation: bridging selective attention and working memory. Trends Cogn Sci 16:128–134. CrossRef Medline
29. Gogulski J, Boldt R, Savolainen P, Guzmán-López J, Carlson S, Pertovaara A (2015) A segregated neural pathway for prefrontal top-down control of tactile discrimination. Cereb Cortex 25:161–166. CrossRef Medline
30. Gramfort A, Luessi M, Larson E, Engemann DA, Strohmeier D, Brodbeck C, Parkkonen L, Hämäläinen MS (2014) MNE software for processing MEG and EEG data. Neuroimage 86:446–460. CrossRef Medline
31. Green JJ, McDonald JJ (2008) Electrical neuroimaging reveals timing of attentional control activity in human brain. PLoS Biol 6:e81. CrossRef
32. Haegens S, Nácher V, Hernández A, Luna R, Jensen O, Romo R (2011) Beta oscillations in the monkey sensorimotor network reflect somatosensory decision making. Proc Natl Acad Sci U S A 108:10708–10713. CrossRef Medline
33. Hämäläinen MS, Ilmoniemi RJ (1994) Interpreting magnetic fields of the brain: minimum norm estimates. Med Biol Eng Comput 32:35–42. CrossRef Medline
34. 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
35. 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
36. Hillebrand A, Barnes GR (2002) A quantitative assessment of the sensitivity of whole-head MEG to activity in the adult human cortex. Neuroimage 16:638–650. CrossRef Medline
37. Hirose S, Watanabe T, Wada H, Imai Y, Machida T, Shirouzu I, Miyashita Y, Konishi S (2013) Functional relevance of micromodules in the human association cortex delineated with high-resolution fMRI. Cereb Cortex 23:2863–2871. CrossRef Medline
38. Hwang K, Ghuman AS, Manoach DS, Jones SR, Luna B (2014) Cortical neurodynamics of inhibitory control. J Neurosci 34:9551–9561. CrossRef Medline
39. Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:1–8. CrossRef Medline
40. Jones SR, Pritchett DL, Stufflebeam SM, Hämäläinen M, Moore CI (2007) Neural correlates of tactile detection: a combined magnetoencephalography and biophysically based computational modeling study. J Neurosci 27:10751–10764. CrossRef Medline
41. 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
42. 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
43. Jovicich J, Czanner S, Greve D, Haley E, van der Kouwe A, Gollub R, Kennedy D, Schmitt F, Brown G, Macfall J, Fischl B, Dale A (2006) Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage 30:436–443. CrossRef Medline
44. Kerr CE, Jones SR, Wan Q, Pritchett DL, Wasserman RH, Wexler A, Villanueva JJ, Shaw JR, Lazar SW, Kaptchuk TJ, Littenberg R, Hamalainen MS, Moore CI (2011) Effects of mindfulness meditation training on anticipatory alpha modulation in primary somatosensory cortex. Brain Res Bull 85:96–103. CrossRef Medline
45. Kerr CE, Sacchet MD, Lazar SW, Moore CI, Jones SR (2013) Mindfulness starts with the body: somatosensory attention and cortical alpha modulation in mindfulness mediation. Front Hum Neurosci 12:1–15. CrossRef Medline
46. Klimesch W (2012) Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 16:606–617. CrossRef Medline
47. Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition–timing hypothesis. Brain Res Rev 53:63–88. CrossRef Medline
48. Kühn AA, Williams D, Kupsch A, Limousin P, Hariz M, Schneider GH, Yarrow K, Brown P (2004) Event-related beta desynchronization in human subthalamic nucleus correlates with motor performance. Brain 127: 735–746. CrossRef Medline
49. Kveraga K, Ghuman AS, Kassam KS, Aminoff EA, Hämäläinen MS, Chaumon M, Bar M (2011) Early onset of neural synchronization in the contextual associations network. Proc Natl Acad Sci U S A 108:3389–3394. CrossRef Medline
50. Lachaux JP, Rodriguez E, Martinerie J, Varela FJ (1999) Measuring phase synchrony in brain signals. Hum Brain Mapp 8:194–208. CrossRef Medline
51. Leek MR (2001) Adaptive procedures in psychophysical research. Percept Psychophys 63:1279–1292. CrossRef Medline
52. Leventhal DK, Gage GJ, Schmidt R, Pettibone JR, Case AC, Berke JD (2012) Basal ganglia beta oscillations accompany cue utilization. Neuron 73:523–536. CrossRef Medline
53. 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
54. Lin FH, Belliveau JW, Dale AM, Hämäläinen MS (2006) Distributed current estimates using cortical orientation constraints. Hum Brain Mapp 27:1–13. CrossRef Medline
55. Liu AK, Dale AM, Belliveau JW (2002) Monte Carlo simulation studies of EEG and MEG localization accuracy. Hum Brain Mapp 16:47–62. CrossRef Medline
56. Miller KJ, Hermes D, Honey CJ, Hebb AO, Ramsey NF, Knight RT, Ojemann JG, Fetz EE (2012) Human motor cortical activity is selectively phaseentrained on underlying rhythms. PLoS Comput Biol 8:e1002655. CrossRef Medline
57. Mosher JC, Leahy RM, Lewis PS (1999) EEG and MEG: forward solutions for inverse methods. IEEE Trans Biomed Eng 46:245–259. CrossRef Medline
58. Nakamura A, Yamada T, Goto A, Kato T, Ito K, Abe Y, Kachi T, Kakigi R (1998) Somatosensory homunculus as drawn by MEG. Neuroimage 7:377–386. CrossRef Medline
59. Neubert FX, Mars RB, Buch ER, Olivier E, Rushworth MF (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
60. Nolte G, Bai O, Wheaton L, Mari Z, Vorbach S, Hallett M (2004) Identifying true brain interaction from EEG data using the imaginary part of coherency. Clin Neurophysiol 115:2292–2307. CrossRef Medline
61. Sadaghiani S, Scheeringa R, Lehongre K, Morillon B, Giraud AL, D’Esposito M, Kleinschmidt A (2012) Alpha-band phase synchrony is related to activity in the fronto-parietal adaptive control network. J Neurosci 32: 14305–14310. CrossRef Medline
62. Sakai K, Passingham RE (2003) Prefrontal interactions reflect future task operations. Nat Neurosci 6:75–81. CrossRef Medline
63. Sauseng P, Klimesch W, Stadler W, Schabus M, Doppelmayr M, Hanslmayr S, Gruber WR, Birbaumer N (2005) A shift of visual spatial attention is selectively associated with human EEG alpha activity. Eru J Neurosci 22:2917–2926. CrossRef Medline
64. Schmiedt JT, Maier A, Fries P, Saunders RC, Leopold DA, Schmid MC (2014) Beta oscillation dynamics in extrastriate cortex after removal of primary visual cortex. J Neurosci 34:11857–11864. CrossRef Medline
65. Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9–18. CrossRef Medline
66. 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
67. Siegel M, Donner TH, Oostenveld R, Fries P, Engel AK (2008) Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron 60:709–719. CrossRef Medline
68. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Net Rev Neurosci 13:120–134. CrossRef Medline
69. Swann N, Poizner H, Houser M, Gould S, Greenhouse I, Cai W, Strunk J, George J, Aron AR (2011) Deep brain stimulation of the subthalamic nucleus alters the cortical profile of response inhibition in the beta frequency band: a scalp EEG study in Parkinson’s disease. J Neurosci 31: 5721–5729. CrossRef Medline
70. 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
71. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, DiSano 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
72. Taulu S, Simola J, Kajola M (2005) Applications of the signal space separation method IEEE Trans Signal Process 53:3359–3372.
73. Tiihonen J, Kajola M, Hari R (1989) Magnetic mu rhythm in man. Neuroscience 32:793–800. CrossRef Medline
74. van Ede F, de Lange FP, Maris E (2012) Attentional cues affect accuracy and reaction time via different cognitive and neural processes. J Neurosci 32:10408–10412. CrossRef Medline
75. Wan Q, Kerr C, Pritchett D, Hämäläinen M, Moore C, Jones S (2011) Dynamics of dynamics within a single data acquisition session: variation in neocortical alpha oscillations in human MEG. PLoS One 6:e24941. CrossRef Medline
76. Weissman DH, Prado J (2012) Heightened activity in a key region of the ventral attention network is linked to reduced activity in a key region of the dorsal attention network during unexpected shifts of covert visual spatial attention. Neuroimage 61:798–804. CrossRef Medline
77. Wessel JR, Conner CR, Aron AR, Tandon N (2013) Chronometric electrical stimulation of right inferior frontal cortex increases motor braking. J Neurosci 33:19611–19619. CrossRef Medline
78. Womelsdorf T, Ardid S, Everling S, Valiante TA (2014) Burst firing synchronizes prefrontal and anterior cingulate cortex during attentional control. Curr Biol 24:2613–2621. CrossRef Medline
79. 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 20:1–6. Medline
80. Zanto TP, Rubens MT, Thangavel A, Gazzaley A (2011) Causal role of the prefrontal cortex in top-down modulation of visual processing and working memory. Nat Neurosci 14:656–661. CrossRef Medline
81. Ziegler DA, Pritchett DL, Hosseini-Varnamkhasti P, Corkin S, Hämäläinen M, Moore CI, Jones SR (2010) Transformations in oscillatory activity and evoked responses in primary somatosensory cortex in middle age: a combined computational neural modeling and MEG study. Neuroimage 52:897–912. CrossRef Medline