The impact of body posture on intrinsic brain activity: The role of beta power at rest


Autoři: Brunella Donno aff001;  Daniele Migliorati aff001;  Filippo Zappasodi aff001;  Mauro Gianni Perrucci aff001;  Marcello Costantini aff002
Působiště autorů: Department of Neuroscience, Imaging and Clinical Sciences, University “G. d’Annunzio” of Chieti, Chieti, Italy aff001;  Institute for Advanced Biomedical Technologies (ITAB), University “G. d’Annunzio” of Chieti, Chieti, Italy aff002;  Center for Biomedical Brain Imaging, University of Delaware, Newark, Delaware, United States of America aff003;  Department of Psychological, Health, and Territorial Sciences, 'G. d'Annunzio” University of Chieti-Pescara, Italy aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0218977

Souhrn

Tying the hands behind the back has detrimental effects on sensorimotor perceptual tasks. Here we provide evidence that beta band oscillatory activity in a resting state condition might play a crucial role in such detrimental effects. EEG activity at rest was measured from thirty young participants (mean age = 24.03) in two different body posture conditions. In one condition participants were required to keep their hands freely resting on the table. In the other condition, participants’ hands were tied behind their back. Increased beta power was observed in the left inferior frontal gyrus during the tied hands condition compared to the free hands condition. A control experiment ruled out alternative explanations for observed change in beta power, including muscle tension. Our findings provide new insights on how body postural manipulations impact on perceptual tasks and brain activity.

Klíčová slova:

Electroencephalography – Electrophysiology – Hands – Muscle contraction – Musculoskeletal system – Scalp – Sensory perception – Vision


Zdroje

1. Shapiro L. Embodied cognition: Routledge; 2010.

2. Rowlands M. The new science of the mind: From extended mind to embodied phenomenology: Mit Press; 2010.

3. Wilson RA, Foglia L. Embodied cognition. 2011.

4. Bonda E, Petrides M, Frey S, EvANs A. Neural correlates of mental transformations of the body-in-space. Proceedings of the National Academy of Sciences. 1995;92(24):11180–4.

5. Cohen RG, Rosenbaum DA. Prospective and retrospective effects in human motor control: planning grasps for object rotation and translation. Psychological Research. 2011;75(4):341–9. doi: 10.1007/s00426-010-0311-6 20941504

6. Ionta S, Perruchoud D, Draganski B, Blanke O. Body context and posture affect mental imagery of hands. PloS one. 2012;7(3):e34382. doi: 10.1371/journal.pone.0034382 22479618

7. Overney LS, Michel CM, Harris IM, Pegna AJ. Cerebral processes in mental transformations of body parts: recognition prior to rotation. Cognitive brain research. 2005;25(3):722–34. doi: 10.1016/j.cogbrainres.2005.09.024 16288855

8. Ionta S, Blanke O. Differential influence of hands posture on mental rotation of hands and feet in left and right handers. Experimental brain research. 2009;195(2):207–17. doi: 10.1007/s00221-009-1770-0 19326106

9. Lopez C, Bachofner C, Mercier M, Blanke O. Gravity and observer's body orientation influence the visual perception of human body postures. Journal of vision. 2009;9(5):1–.

10. Dijkstra K, Kaschak MP, Zwaan RA. Body posture facilitates retrieval of autobiographical memories. Cognition. 2007;102(1):139–49. doi: 10.1016/j.cognition.2005.12.009 16472550

11. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME. The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences. 2005;102(27):9673–8.

12. Thibault RT, Lifshitz M, Raz A. Body position alters human resting-state: Insights from multi-postural magnetoencephalography. Brain imaging and behavior. 2016;10(3):772–80. doi: 10.1007/s11682-015-9447-8 26409469

13. Pfurtscheller G, Aranibar A. Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. Electroencephalography and clinical neurophysiology. 1979;46(2):138–46. doi: 10.1016/0013-4694(79)90063-4 86421

14. Herrmann CS, Munk MH, Engel AK. Cognitive functions of gamma-band activity: memory match and utilization. Trends in cognitive sciences. 2004;8(8):347–55. doi: 10.1016/j.tics.2004.06.006 15335461

15. Martinovic J, Busch NA. High frequency oscillations as a correlate of visual perception. International Journal of Psychophysiology. 2011;79(1):32–8. doi: 10.1016/j.ijpsycho.2010.07.004 20654659

16. Tallon-Baudry C. The roles of gamma-band oscillatory synchrony in human visual cognition. Front Biosci. 2009;14:321–32.

17. Brinkman L, Stolk A, Dijkerman HC, de Lange FP, Toni I. Distinct roles for alpha-and beta-band oscillations during mental simulation of goal-directed actions. Journal of Neuroscience. 2014;34(44):14783–92. doi: 10.1523/JNEUROSCI.2039-14.2014 25355230

18. Cheyne DO. MEG studies of sensorimotor rhythms: a review. Experimental neurology. 2013;245:27–39. doi: 10.1016/j.expneurol.2012.08.030 22981841

19. Hari R, Salmelin R. Human cortical oscillations: a neuromagnetic view through the skull. Trends in neurosciences. 1997;20(1):44–9. doi: 10.1016/S0166-2236(96)10065-5 9004419

20. Jensen O, Goel P, Kopell N, Pohja M, Hari R, Ermentrout B. On the human sensorimotor-cortex beta rhythm: sources and modeling. Neuroimage. 2005;26(2):347–55. doi: 10.1016/j.neuroimage.2005.02.008 15907295

21. Natraj N, Poole V, Mizelle J, Flumini A, Borghi AM, Wheaton LA. Context and hand posture modulate the neural dynamics of tool–object perception. Neuropsychologia. 2013;51(3):506–19. doi: 10.1016/j.neuropsychologia.2012.12.003 23261936

22. Zimmermann M, Toni I, de Lange FP. Body posture modulates action perception. Journal of Neuroscience. 2013;33(14):5930–8. doi: 10.1523/JNEUROSCI.5570-12.2013 23554475

23. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. Journal of neuroscience methods. 2004;134(1):9–21. doi: 10.1016/j.jneumeth.2003.10.009 15102499

24. Hyvärinen A, Oja E. Independent component analysis: algorithms and applications. Neural networks. 2000;13(4–5):411–30. doi: 10.1016/s0893-6080(00)00026-5 10946390

25. Goncharova II, McFarland DJ, Vaughan TM, Wolpaw JR. EMG contamination of EEG: spectral and topographical characteristics. Clinical neurophysiology. 2003;114(9):1580–93. doi: 10.1016/s1388-2457(03)00093-2 12948787

26. Zakeri Z, Assecondi S, Bagshaw A, Arvanitis T, editors. Influence of signal preprocessing on ICA-based EEG decomposition. XIII Mediterranean Conference on Medical and Biological Engineering and Computing 2013; 2014: Springer.

27. Fell J, Widman G, Rehberg B, Elger CE, Fernandez G. Human mediotemporal EEG characteristics during propofol anesthesia. Biological cybernetics. 2005;92(2):92–100. doi: 10.1007/s00422-004-0538-7 15685392

28. Oostenveld R, Fries P, Maris E, Schoffelen J-M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Computational intelligence and neuroscience. 2011;2011:1. doi: 10.1155/2011/720971

29. Pascual-Marqui RD. Discrete, 3D distributed, linear imaging methods of electric neuronal activity. Part 1: exact, zero error localization. arXiv preprint arXiv:07103341. 2007.

30. Creem-Regehr SH, Lee JN. Neural representations of graspable objects: are tools special? Cognitive Brain Research. 2005;22(3):457–69. doi: 10.1016/j.cogbrainres.2004.10.006 15722215

31. Arnstein D, Cui F, Keysers C, Maurits NM, Gazzola V. μ-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. Journal of Neuroscience. 2011;31(40):14243–9. doi: 10.1523/JNEUROSCI.0963-11.2011 21976509

32. Cochin S, Barthelemy C, Lejeune B, Roux S, Martineau J. Perception of motion and qEEG activity in human adults. Electroencephalography and clinical neurophysiology. 1998;107(4):287–95. doi: 10.1016/s0013-4694(98)00071-6 9872446

33. Frenkel-Toledo S, Bentin S, Perry A, Liebermann DG, Soroker N. Dynamics of the EEG power in the frequency and spatial domains during observation and execution of manual movements. Brain research. 2013;1509:43–57. doi: 10.1016/j.brainres.2013.03.004 23500633

34. Hari R, Forss N, Avikainen S, Kirveskari E, Salenius S, Rizzolatti G. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proceedings of the National Academy of Sciences. 1998;95(25):15061–5.

35. Perry A, Bentin S. Mirror activity in the human brain while observing hand movements: A comparison between EEG desynchronization in the μ-range and previous fMRI results. Brain research. 2009;1282:126–32. doi: 10.1016/j.brainres.2009.05.059 19500557

36. Caggiano V, Fogassi L, Rizzolatti G, Thier P, Casile A. Mirror neurons differentially encode the peripersonal and extrapersonal space of monkeys. science. 2009;324(5925):403–6. doi: 10.1126/science.1166818 19372433

37. Cisek P, Kalaska JF. Neural mechanisms for interacting with a world full of action choices. Annual review of neuroscience. 2010;33:269–98. doi: 10.1146/annurev.neuro.051508.135409 20345247

38. Proverbio AM. Tool perception suppresses 10–12Hz μ rhythm of EEG over the somatosensory area. Biological psychology. 2012;91(1):1–7. doi: 10.1016/j.biopsycho.2012.04.003 22543070

39. Proverbio AM, Adorni R, D’Aniello GE. 250ms to code for action affordance during observation of manipulable objects. Neuropsychologia. 2011;49(9):2711–7. doi: 10.1016/j.neuropsychologia.2011.05.019 21664367

40. Pfurtscheller G, Da Silva FL. Event-related EEG/MEG synchronization and desynchronization: basic principles. Clinical neurophysiology. 1999;110(11):1842–57. doi: 10.1016/s1388-2457(99)00141-8 10576479

41. Salmelin R, Hámáaláinen M, Kajola M, Hari R. Functional segregation of movement-related rhythmic activity in the human brain. Neuroimage. 1995;2(4):237–43. doi: 10.1006/nimg.1995.1031 9343608

42. Baker S, Olivier E, Lemon R. Coherent oscillations in monkey motor cortex and hand muscle EMG show task‐dependent modulation. The Journal of physiology. 1997;501(1):225–41.

43. Zavala B, Zaghloul K, Brown P. The subthalamic nucleus, oscillations, and conflict. Movement Disorders. 2015;30(3):328–38. doi: 10.1002/mds.26072 25688872

44. Swann N, Tandon N, Canolty R, Ellmore TM, McEvoy LK, Dreyer S, et al. Intracranial EEG reveals a time-and frequency-specific role for the right inferior frontal gyrus and primary motor cortex in stopping initiated responses. Journal of Neuroscience. 2009;29(40):12675–85. doi: 10.1523/JNEUROSCI.3359-09.2009 19812342

45. Androulidakis AG, Doyle LM, Yarrow K, Litvak V, Gilbertson TP, Brown P. Anticipatory changes in beta synchrony in the human corticospinal system and associated improvements in task performance. European Journal of Neuroscience. 2007;25(12):3758–65. doi: 10.1111/j.1460-9568.2007.05620.x 17610595

46. Joundi RA, Jenkinson N, Brittain J-S, Aziz TZ, Brown P. Driving oscillatory activity in the human cortex enhances motor performance. Current Biology. 2012;22(5):403–7. doi: 10.1016/j.cub.2012.01.024 22305755

47. Feurra M, Bianco G, Santarnecchi E, Del Testa M, Rossi A, Rossi S. Frequency-dependent tuning of the human motor system induced by transcranial oscillatory potentials. Journal of Neuroscience. 2011;31(34):12165–70. doi: 10.1523/JNEUROSCI.0978-11.2011 21865459

48. Pogosyan A, Gaynor LD, Eusebio A, Brown P. Boosting cortical activity at beta-band frequencies slows movement in humans. Current Biology. 2009;19(19):1637–41. doi: 10.1016/j.cub.2009.07.074 19800236

49. Wach C, Krause V, Moliadze V, Paulus W, Schnitzler A, Pollok B. Effects of 10Hz and 20Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability. Behavioural brain research. 2013;241:1–6. doi: 10.1016/j.bbr.2012.11.038 23219965

50. Brown P. Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Current opinion in neurobiology. 2007;17(6):656–64. doi: 10.1016/j.conb.2007.12.001 18221864

51. Jenkinson N, Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends in neurosciences. 2011;34(12):611–8. doi: 10.1016/j.tins.2011.09.003 22018805

52. Engel AK, Fries P. Beta-band oscillations—signalling the status quo? Current opinion in neurobiology. 2010;20(2):156–65. doi: 10.1016/j.conb.2010.02.015 20359884

53. Jeannerod M, Arbib MA, Rizzolatti G, Sakata H. Grasping objects: the cortical mechanisms of visuomotor transformation. Trends in neurosciences. 1995;18(7):314–20. 7571012

54. Rizzolatti G, Gentilucci M. Motor and visual-motor functions of the premotor cortex. Neurobiology of neocortex. 1988;42:269–84.

55. Buccino G, Binkofski F, Fink GR, Fadiga L, Fogassi L, Gallese V, et al. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European journal of neuroscience. 2001;13(2):400–4. 11168545

56. Calvo-Merino B, Grèzes J, Glaser DE, Passingham RE, Haggard P. Seeing or doing? Influence of visual and motor familiarity in action observation. Current Biology. 2006;16(19):1905–10. doi: 10.1016/j.cub.2006.07.065 17027486

57. Galati G, Committeri G, Spitoni G, Aprile T, Di Russo F, Pitzalis S, et al. A selective representation of the meaning of actions in the auditory mirror system. Neuroimage. 2008;40(3):1274–86. doi: 10.1016/j.neuroimage.2007.12.044 18276163

58. Grafton ST, Arbib MA, Fadiga L, Rizzolatti G. Localization of grasp representations in humans by positron emission tomography. Experimental brain research. 1996;112(1):103–11. doi: 10.1007/bf00227183 8951412

59. Ortigue S, Sinigaglia C, Rizzolatti G, Grafton ST. Understanding actions of others: the electrodynamics of the left and right hemispheres. A high-density EEG neuroimaging study. PloS one. 2010;5(8):e12160. doi: 10.1371/journal.pone.0012160 20730095

60. Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Cognitive brain research. 1996;3(2):131–41. doi: 10.1016/0926-6410(95)00038-0 8713554

61. Swick D, Ashley V, Turken U. Left inferior frontal gyrus is critical for response inhibition. BMC neuroscience. 2008;9(1):102.

62. Buccino G, Sato M, Cattaneo L, Rodà F, Riggio L. Broken affordances, broken objects: a TMS study. Neuropsychologia. 2009;47(14):3074–8. doi: 10.1016/j.neuropsychologia.2009.07.003 19615389

63. Chao LL, Martin A. Representation of manipulable man-made objects in the dorsal stream. Neuroimage. 2000;12(4):478–84. doi: 10.1006/nimg.2000.0635 10988041

64. Grafton ST, Fadiga L, Arbib MA, Rizzolatti G. Premotor cortex activation during observation and naming of familiar tools. Neuroimage. 1997;6(4):231–6. doi: 10.1006/nimg.1997.0293 9417966

65. Grèzes J, Tucker M, Armony J, Ellis R, Passingham RE. Objects automatically potentiate action: an fMRI study of implicit processing. European Journal of Neuroscience. 2003;17(12):2735–40. doi: 10.1046/j.1460-9568.2003.02695.x 12823480

66. Johnson-Frey SH, Newman-Norlund R, Grafton ST. A distributed left hemisphere network active during planning of everyday tool use skills. Cerebral cortex. 2004;15(6):681–95. doi: 10.1093/cercor/bhh169 15342430


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