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Top-down modulation of brain activity underlying intentional action and its relationship with awareness of intention: an ERP/Laplacian analysis

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Abstract

Intentional actions are executed with the peculiar experience of “I decide to do that.” It has been proposed that intentional actions involve a specific brain network involving the supplementary motor areas (SMAs). Here, we manipulated the internal representation participants attended to (intention vs. movement) in order to (1) examine the activity of SMAs and of the primary motor cortex (M1) during intentional action preparation and execution, and (2) investigate the temporal relationship between activity in these structures and intention awareness. Participants performed self-paced key presses. After each key press, participants were asked to report either the time they had the first intention to press the key (W-condition) or the time they actually started the movement (M-condition). We then estimated surface Laplacians from brain electrical potentials recorded while participants were performing the task. Activity in SMAs was greater in the W-condition than in the M-condition more than 1 s before electromyographic (EMG) activation, suggesting that this region is indeed associated to the formation of conscious intention. Conversely, activity in primary motor cortex (M1) contralateral to the responding hand was larger in the M-condition than in the W-condition, revealing that this region is also modulated by top-down processes. In addition, waveforms time-locked to the W-judgement revealed that M1 as well as EMG activation preceded the time at which participants become aware of their intention by about 0.3 s. This observation argues against the possibility that the temporal delay between motor-related activation and intention awareness results from smearing artifacts.

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References

  • Banks WP, Isham E (2009) We infer rather than perceive the moment we decided to act. Psychol Sci 20:17–21

    Article  PubMed  Google Scholar 

  • Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neurosci 14:319–325

    Google Scholar 

  • Callaway E, Halliday R, Naylor H, Thouvenin D (1984) The latency of the average is not the average of the latencies. Psychophysiology 21:571

    Google Scholar 

  • Cui RQ, Huter D, Lang W, Deecke L (1999) Neuroimage of voluntary movement: topography of the Bereitschaftspotential, a 64-channel DC current source density study. NeuroImage 9:124–134

    Article  PubMed  CAS  Google Scholar 

  • Danquah AN, Farrell MJ, O’Boyle DJ (2008) Biases in the subjective timing of perceptual events: Libet et al. (1983) revisited. Conscious Cogn 17:616–627

    Article  PubMed  Google Scholar 

  • Desmurget M, Sirigu A (2009) A parietal-premotor network for movement intention and motor awareness. Trends Cogn Sci 13:411–419

    Article  PubMed  Google Scholar 

  • Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813

    Article  PubMed  CAS  Google Scholar 

  • Eagleman DM (2004) The where and when of intention. Science 303:1144–1146

    Article  PubMed  CAS  Google Scholar 

  • Gomes G (1998) The timing of conscious experience: a critical review and reinterpretation of Libet’s research. Conscious Cogn 7:559–595

    Article  PubMed  CAS  Google Scholar 

  • Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484

    Article  PubMed  CAS  Google Scholar 

  • Griffin IC, Nobre AC (2003) Orienting attention to locations in internal representations. J Cogn Neurosci 15:1176–1194

    Article  PubMed  Google Scholar 

  • Guggisberg AG, Dalal SS, Schnider A, Nagarajana SS (2011) The neural basis of event-time introspection. Conscious Cogn 20:1899–1915

    Article  PubMed  Google Scholar 

  • Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9:934–946

    Article  PubMed  CAS  Google Scholar 

  • Haggard P, Eimer M (1999) On the relation between brain potentials and the awareness of voluntary movements. Exp Brain Res 126:128–133

    Article  PubMed  CAS  Google Scholar 

  • Haggard P, Clark S, Kalogeras J (2002) Voluntary action and conscious awareness. Nat Neurosci 5:382–385

    Article  PubMed  CAS  Google Scholar 

  • Hallett M (2007) Volitional control of movement: the physiology of free will. Clin Neurophysiol 118:1179–1192

    Article  PubMed  Google Scholar 

  • Jasper HH (1958) Report of committee on methods of clinical examination in electroencephalography. Electroencephalogr Clin Neurophysiol 10:370–375

    Article  Google Scholar 

  • Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341

    Article  PubMed  CAS  Google Scholar 

  • Keller I, Heckhausen B (1990) Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control. Electroencephalogr Clin Neurophysiol 76:351–361

    Article  PubMed  CAS  Google Scholar 

  • Keller PE, Wascher E, Prinz W, Waszak F, Koch I, Rosenbaum DA (2006) Differences between intention-based and stimulus-based actions. J Psychophysiol 20:9–20

    Article  Google Scholar 

  • Kitamura J, Shibasaki H, Kondo T (1993) A cortical slow potential is larger before an isolated movement of a single finger than simultaneous movement of two fingers. Electroencephalogr Clin Neurophysiol 86:252–258

    Article  PubMed  CAS  Google Scholar 

  • Kornhuber HH, Deecke L (1965) Hirnpotentialänderungen bei Willkurbewegungen und passive Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflügers Archiv für die Gesamte Physiologie des Menschen und der Tiere 284:1–17

    Article  PubMed  CAS  Google Scholar 

  • Krieghoff V, Waszak F, Prinz W, Brass M (2011) Neural and behavioral correlates of intentional actions. Neuropsychologia 49:767–776

    Article  PubMed  Google Scholar 

  • Lau HC, Rogers RD, Haggard P, Passingham RE (2004) Attention to intention. Science 303:1208–1210

    Article  PubMed  CAS  Google Scholar 

  • Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90

    Article  PubMed  Google Scholar 

  • Law SK, Rohrbaugh JW, Adams CM, Eckardt MJ (1993) Improving spatial and temporal resolution in evoked EEG responses using surface Laplacians. Electroencephal Clin Neurophysiol 88:309–322

    Article  CAS  Google Scholar 

  • Libet B, Wright EW, Gleason CA (1982) Readiness-potentials preceding unrestricted ‘spontaneous’ vs. pre-planned voluntary acts. Electroenceph Clin Neurophysiol 54:322–335

    Google Scholar 

  • Libet B, Gleason CA, Wright EW, Pearl DK (1983) Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 106:623–642

    Article  PubMed  Google Scholar 

  • Macar F, Vidal F, Casini L (1999) The supplementary motor area in motor and sensory timing: evidence from slow brain potential changes. Exp Brain Res 125:271–280

    Article  PubMed  CAS  Google Scholar 

  • Matsuhashi M, Hallett M (2008) The timing of the conscious intention to move. Eur J Neurosci 28:2344–2351

    Article  PubMed  Google Scholar 

  • Meyer DE, Osman AM, Irwin DE, Yantis S (1988) Modern mental chronometry. Biol Psychol 26:3–67

    Article  PubMed  CAS  Google Scholar 

  • Miller J, Shepherdson P, Trevena J (2011) Effects of clock monitoring on electroencephalographic activity: is unconscious movement initiation an artifact of the clock? Psychol Sci 22:103–109

    Article  PubMed  Google Scholar 

  • Nunez PL (2000) Toward a quantitative description of large scale neocortical dynamic function and EEG. Behav Brain Sci 23:371–398

    Article  PubMed  CAS  Google Scholar 

  • Nunez PL, Srinivasan R (2005) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Perrin F, Pernier J, Bertrand D, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184–187

    Article  PubMed  CAS  Google Scholar 

  • Pockett S, Miller A (2007) The rotating spot method of timing subjective events. Conscious Cogn 16:241–254

    Article  PubMed  Google Scholar 

  • Rigoni D, Brass M, Sartori G (2010) Post-action determinants of the reported time of conscious intentions. Front Hum Neurosci 4:38

    PubMed  Google Scholar 

  • Rigoni D, Kühn S, Sartori G, Brass M (2011) Inducing disbelief in free will alters brain correlates of preconscious motor preparation: the brain minds whether we believe in free will or not. Psychol Sci 22:613–618

    Article  PubMed  Google Scholar 

  • Roskies AL (2010) How does neuroscience affect our conception of volition? Annu Rev Neurosci 33:109–130

    Article  PubMed  CAS  Google Scholar 

  • Schurger A, Sitt JD, Dehaene S (2012) An accumulator model for spontaneous neural activity prior to self-initiated movement. Proc Natl Acad Sci USA 109:E2904–E2913

    Google Scholar 

  • Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356

    Article  PubMed  Google Scholar 

  • Shibasaki H, Barrett G, Halliday H, Halliday AM (1980) Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol 49:213–226

    Article  PubMed  CAS  Google Scholar 

  • Sirigu A, Daprati E, Ciancia S, Giraux P, Nighoghossian N (2004) Altered awareness of voluntary action after damage to the parietal cortex. Nature 7:80–84

    CAS  Google Scholar 

  • Staude G, Flachenecker C, Daumer M, Wolf W (2001) Onset detection in surface electromyographic signals: a systematic comparison of methods. J Appl Sign Process 2:67–81

    Article  Google Scholar 

  • Steinmetz H, Fürst G, Meyer BH (1989) Craniocerebral topography within the international 10–20 system. Electroencephalogr Clin Neurophysiol 72:499–506

    Article  PubMed  CAS  Google Scholar 

  • Taylor M (1978) Bereitschaftspotential during the acquisition of a skilled motor task. Electroencephalogr Clin Neurophysiol 45:568–576

    Article  PubMed  CAS  Google Scholar 

  • Trevena J, Miller J (2002) Cortical movement preparation before and after a conscious decision to move. Conscious Cogn 11:162–190

    Article  PubMed  Google Scholar 

  • Trevena J, Miller J (2010) Brain preparation before a voluntary action: evidence against unconscious movement initiation. Conscious Cogn 19:447–456

    Article  PubMed  Google Scholar 

  • Van Boxtel GJM, Geraats LHD, Van den Berg-Lessen MMC, Brunia CHM (1993) Detection of EMG onset in ERP research. Psychophysiology 30:405–412

    Article  PubMed  Google Scholar 

  • Vidal F, Bonnet M, Macar F (1995) Programming the duration of a motor sequence: role of the primary and supplementary motor areas in man. Exp Brain Res 106:339–350

    Article  PubMed  CAS  Google Scholar 

  • Vidal F, Grapperon J, Bonnet M, Hasbroucq T (2003) The nature of unilateral motor commands in between-hand choice tasks as revealed by surface Laplacian estimation. Psychophysiology 40:796–805

    Article  PubMed  Google Scholar 

  • Waszak F, Wascher E, Keller P, Koch I, Aschersleben G, Rosenbaum DA, Prinz W (2005) Intention-based and stimulus-based mechanisms in action selection. Exp Brain Res 162:346–356

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the Centro Universitario Internazionale, Monte San Savino, Italy, and the Cassa di Risparmio di Padova e Rovigo (Cariparo), Italy. The authors would like to thank Sandro Bettella for technical support, Boris Burle and Dimitrios Kourtis for their helpful comments.

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Correspondence to Davide Rigoni.

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221_2013_3400_MOESM1_ESM.tiff

Laplacian surface estimates and EMG traces, time-locked to the W-judgment, for each participant. The black solid line indicates the W-judgment. The left y-axis indicates the amplitude for the surface Laplacian estimates, and the right y-axis marks the amplitude for the EMG signal. (TIFF 760 kb)

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Rigoni, D., Brass, M., Roger, C. et al. Top-down modulation of brain activity underlying intentional action and its relationship with awareness of intention: an ERP/Laplacian analysis. Exp Brain Res 229, 347–357 (2013). https://doi.org/10.1007/s00221-013-3400-0

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  • DOI: https://doi.org/10.1007/s00221-013-3400-0

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