Reciprocal interactions of the SMA and cingulate cortex sustain premovement activity for voluntary actions

Journal of Neuroscience

Volumn 34, Issue 49, 2014, Pages 16397-16407

  Nguyen, Vinh T ^a,b   Breakspear, Michael ^b,c,d,e   Cunnington, Ross ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

^d BLACK DOG INSTITUTE   (Australia)

^e ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

Anterior mid cingulate cortex; Multimodal data fusion; Readiness potential; Simultaneous EEG fMRI; Supplementary motor area; Voluntary action

Indexed keywords

ADULT; AMPLITUDE MODULATION; ANTERIOR CINGULATE; ARTICLE; BRAIN FUNCTION; CONNECTOME; CONTINGENT NEGATIVE VARIATION; DEFAULT MODE NETWORK; ELECTROENCEPHALOGRAPHY; EVOKED CORTICAL RESPONSE; EYE MOVEMENT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; INDEPENDENT COMPONENT ANALYSIS; LEFT HEMISPHERE; MALE; NERVE CONDUCTION; NERVE POTENTIAL; NEUROMODULATION; PRIMARY MOTOR CORTEX; RIGHT HEMISPHERE; SUPPLEMENTARY MOTOR AREA; VOLUNTARY MOVEMENT; BIOLOGICAL MODEL; BRAIN MAPPING; CINGULATE GYRUS; ELECTROENCEPHALOGRAM; MOTOR CORTEX; MOVEMENT (PHYSIOLOGY); NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PHYSIOLOGY; YOUNG ADULT;

ADULT; BRAIN MAPPING; BRAIN WAVES; CONTINGENT NEGATIVE VARIATION; ELECTROENCEPHALOGRAPHY; FEMALE; GYRUS CINGULI; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MODELS, NEUROLOGICAL; MOTOR CORTEX; MOVEMENT; NEURAL PATHWAYS; YOUNG ADULT;

EID: 84914674446     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2571-14.2014     Document Type: Article

References (59)

1. Aburn MJ, Holmes CA, Roberts JA, Boonstra TW, Breakspear M (2012) Critical fluctuations in cortical models near instability. Front Physiol 3:331. CrossRef Medline
2. Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12:230-239. CrossRef Medline
3. Ball T, Schreiber A, Feige B, Wagner M, Lücking CH, Kristeva-Feige R (1999) The role of higher-order motor areas in voluntary movement as revealed by high-resolution EEG and fMRI. Neuroimage 10:682-694. CrossRef Medline
4. Breakspear M (2002) Nonlinear phase desynchronization in human electroencephalographic data. Hum Brain Mapp 15:175-198. CrossRef Medline
5. Breakspear M, Terry JR, Friston KJ (2003) Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a biophysical model of neuronal dynamics. Network 14:703-732. CrossRef Medline
6. Brotchie P, Iansek R, Horne MK (1991) Motor function of the monkey globus pallidus. 2. Cognitive aspects of movement and phasic neuronal activity. Brain 114:1685-1702. CrossRef Medline
7. Cerutti S, Baselli G, Liberati D, Pavesi G (1987) Single sweep analysis of visual evoked potentials through a model of parametric identification. Biol Cybern 56:111-120. CrossRef Medline
8. Cunnington R, Iansek R, Bradshaw JL, Phillips JG (1995) Movementrelated potentials in Parkinson’s disease. Presence and predictability of temporal and spatial cues. Brain 118:935-950. CrossRef Medline
9. Cunnington R, Iansek R, Johnson KA, Bradshaw JL (1997) Movementrelated potentials in Parkinson’s disease. Motor imagery and movement preparation. Brain 120:1339-1353. CrossRef Medline
10. Cunnington R, Windischberger C, Deecke L, Moser E (2002) The preparation and execution of self-initiated and externally-triggered movement: a study of event-related fMRI. Neuroimage 15:373-385. CrossRef Medline
11. Cunnington R, Windischberger C, Deecke L, Moser E (2003) The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response. Neuroimage 20:404-412. CrossRef Medline
12. Cunnington R, Windischberger C, Moser E (2005) Premovement activity of the presupplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. Hum Mov Sci 24:644-656. CrossRef Medline
13. Cunnington R, Windischberger C, Robinson S, Moser E (2006) The selection of intended actions and the observation of others’ actions: a timeresolved fMRI study. Neuroimage 29:1294-1302. CrossRef Medline
14. Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel AK (2005) Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25:11730-11737. CrossRef Medline
15. 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
16. Duncan NW, Northoff G (2013) Overview of potential procedural and participant-related confounds for neuroimaging of the resting state. J Psychiatry Neurosci 38:84-96. CrossRef Medline
17. Eichele T, Specht K, Moosmann M, Jongsma ML, Quiroga RQ, Nordby H, Hugdahl K (2005) Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. Proc Natl Acad Sci U S A 102:17798-17803. CrossRef Medline
18. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325-1335. CrossRef Medline
19. Erdler M, Beisteiner R, Mayer D, Kaindl T, Edward V, Windischberger C, Lindinger G, Deecke L (2000) Supplementary motor area activation preceding voluntary movement is detectable with a whole-scalp magnetoencephalography system. Neuroimage 11:697-707. CrossRef Medline
20. Freyer F, Roberts JA, Ritter P, Breakspear M (2012) A canonical model of multistability and scale-invariance in biological systems. PLoS Comput Biol 8:e1002634. CrossRef Medline
21. Friston K (2010) The free-energy principle: a unified brain theory? Nat Rev Neurosci 11:127-138. CrossRef Medline
22. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuroimage 19:1273-1302. CrossRef Medline
23. Friston K, Breakspear M, Deco G (2012) Perception and self-organized instability. Front Comput Neurosci 6:44. CrossRef Medline
24. Grefkes C, Eickhoff SB, Nowak DA, Dafotakis M, Fink GR (2008) Dynamic intra-and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM. Neuroimage 41:1382-1394. CrossRef Medline
25. Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9:934-946. CrossRef Medline
26. Hoffstaedter F, Grefkes C, Zilles K, Eickhoff SB (2013) The “what” and “when” of self-initiated movements. Cereb Cortex 23:520-530. CrossRef Medline
27. Hoffstaedter F, Grefkes C, Caspers S, Roski C, Palomero-Gallagher N, Laird AR, Fox PT, Eickhoff SB (2014) The role of anterior midcingulate cortex in cognitive motor control: evidence from functional connectivity analyses. Hum Brain Mapp 35:2741-2753. CrossRef Medline
28. Jahanshahi M, Jenkins IH, Brown RG, Marsden CD, Passingham RE, Brooks DJ (1995) Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain 118:913-933. CrossRef Medline
29. Jansen M, White TP, Mullinger KJ, Liddle EB, Gowland PA, Francis ST, Bowtell R, Liddle PF (2012) Motion-related artefacts in EEG predict neuronally plausible patterns of activation in fMRI data. Neuroimage 59:261-270. CrossRef Medline
30. Kasess CH, Windischberger C, Cunnington R, Lanzenberger R, Pezawas L, Moser E (2008) The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling. Neuroimage 40: 828-837. CrossRef Medline
31. Kelso JA (2010) Instabilities and phase transitions in human brain and behavior. Front Hum Neurosci 4:23. CrossRef Medline
32. Kornhuber HH, Deecke L (1964) Hirnpotentialanderungen beim Menschen vor und nach Willkurbewegungen, dargestellt mit Magnetbandspeicherung und Ruckwartsanalyse. Pflugers Arch 281:52.
33. Lang W, Cheyne D, Kristeva R, Beisteiner R, Lindinger G, Deecke L (1991) Three-dimensional localization of SMA activity preceding voluntary movement. A study of electric and magnetic fields in a patient with infarction of the right supplementary motor area. Exp Brain Res 87:688-695. CrossRef Medline
34. Lau HC, Rogers RD, Ramnani N, Passingham RE (2004) Willed action and attention to the selection of action. Neuroimage 21:1407-1415. CrossRef Medline
35. Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48:609-621. CrossRef Medline
36. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature 412: 150-157. CrossRef Medline
37. Matsumoto K, Suzuki W, Tanaka K (2003) Neuronal correlates of goalbased motor selection in the prefrontal cortex. Science 301:229-232. CrossRef Medline
38. Moosmann M, Schönfelder VH, Specht K, Scheeringa R, Nordby H, Hugdahl K (2009) Realignment parameter-informed artefact correction for simultaneous EEG-fMRI recordings. Neuroimage 45:1144-1150. CrossRef Medline
39. Mulert C, Seifert C, Leicht G, Kirsch V, Ertl M, Karch S, Moosmann M, Lutz J, Möller H-J, Hegerl U, Pogarell O, Jäger L (2008) Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making. Neuroimage 42:158-168. CrossRef Medline
40. Nguyen VT, Cunnington R (2014) The superior temporal sulcus and the N170 during face processing: single trial analysis of concurrent EEGfMRI. Neuroimage 86:492-502. CrossRef Medline
41. Nguyen VT, Breakspear M, Cunnington R (2013) Fusing concurrent EEGfMRI with dynamic causal modeling: application to effective connectivity during face perception. Neuroimage S1053-8119(13)00730-1.CrossRef
42. Niazy RK, Beckmann CF, Iannetti GD, Brady JM, Smith SM (2005) Removal of FMRI environment artifacts from EEG data using optimal basis sets. Neuroimage 28:720-737. CrossRef Medline
43. Paus T (2001) Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2:417-424. CrossRef Medline
44. Paus T, Petrides M, Evans AC, Meyer E (1993) Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 70:453-469.Medline
45. Penny WD (2012) Comparing dynamic causal models using AIC, BIC and free energy. Neuroimage 59:319-330. CrossRef Medline
46. Picard N, Strick PL (1996) Motor areas of the medial wall: a review of their location and functional activation. Cereb Cortex 6:342-353. CrossRef Medline
47. Pool EM, Rehme AK, Fink GR, Eickhoff SB, Grefkes C (2013) Network dynamics engaged in the modulation of motor behavior in healthy subjects. Neuroimage 82:68-76. CrossRef Medline
48. Praamstra P, Stegeman DF, Horstink MW, Cools AR (1996) Dipole source analysis suggests selective modulation of the supplementary motor area contribution to the readiness potential. Electroencephalogr Clin Neurophysiol 98:468-477. CrossRef Medline
49. Roskies AL (2010) How does neuroscience affect our conception of volition? Annu Rev Neurosci 33:109-130. CrossRef Medline
50. Rushworth MF, Walton M, Kennerley SW, Bannerman DM (2004) Action sets and decisions in the medial frontal cortex. Trends Cogn Sci 8:410-417. CrossRef Medline
51. Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341-2356. CrossRef Medline
52. Shima K, Tanji J (1998) Role for cingulate motor area cells in voluntary movement selection based on reward. Science 282:1335-1338. CrossRef Medline
53. Stephan KE, Marshall JC, Penny WD, Friston KJ, Fink GR (2007) Interhemispheric integration of visual processing during task-driven lateralization. J Neurosci 27:3512-3522. CrossRef Medline
54. Stephan KE, Kasper L, Harrison LM, Daunizeau J, den Ouden HE, Breakspear M, Friston KJ (2008) Nonlinear dynamic causal models for fMRI. Neuroimage 42:649-662. CrossRef Medline
55. Toma K, Matsuoka T, Immisch I, Mima T, Waldvogel D, Koshy B, Hanakawa T, Shill H, Hallett M (2002) Generators of movement-related cortical potentials: fMRI-constrained EEG dipole source analysis. Neuroimage 17:161-173. CrossRef Medline
56. Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15:273-289. CrossRef Medline
57. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31:15775-15786. CrossRef Medline
58. Windischberger C, Cunnington R, Lamm C, Lanzenberger R, Langenberger H, Deecke L, Bauer H, Moser E (2008) Time-resolved analysis of fMRI signal changes using brain activation movies. J Neurosci Methods 169: 222-230. CrossRef Medline
59. Yazawa S, Ikeda A, Kunieda T, Ohara S, Mima T, Nagamine T, Taki W, Kimura J, Hori T, Shibasaki H (2000) Human presupplementary motor area is active before voluntary movement: subdural recording of Bereitschaftspotential from medial frontal cortex. Exp Brain Res 131:165-177. CrossRef Medline