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Published in: Experimental Brain Research 3/2013

01-09-2013 | Research Article

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

Authors: Davide Rigoni, Marcel Brass, Clémence Roger, Franck Vidal, Giuseppe Sartori

Published in: Experimental Brain Research | Issue 3/2013

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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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Literature
go back to reference Banks WP, Isham E (2009) We infer rather than perceive the moment we decided to act. Psychol Sci 20:17–21PubMedCrossRef Banks WP, Isham E (2009) We infer rather than perceive the moment we decided to act. Psychol Sci 20:17–21PubMedCrossRef
go back to reference Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neurosci 14:319–325 Brass M, Haggard P (2008) The what, when, whether model of intentional action. Neurosci 14:319–325
go back to reference Callaway E, Halliday R, Naylor H, Thouvenin D (1984) The latency of the average is not the average of the latencies. Psychophysiology 21:571 Callaway E, Halliday R, Naylor H, Thouvenin D (1984) The latency of the average is not the average of the latencies. Psychophysiology 21:571
go back to reference 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 9:124–134PubMedCrossRef 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 9:124–134PubMedCrossRef
go back to reference Danquah AN, Farrell MJ, O’Boyle DJ (2008) Biases in the subjective timing of perceptual events: Libet et al. (1983) revisited. Conscious Cogn 17:616–627PubMedCrossRef Danquah AN, Farrell MJ, O’Boyle DJ (2008) Biases in the subjective timing of perceptual events: Libet et al. (1983) revisited. Conscious Cogn 17:616–627PubMedCrossRef
go back to reference Desmurget M, Sirigu A (2009) A parietal-premotor network for movement intention and motor awareness. Trends Cogn Sci 13:411–419PubMedCrossRef Desmurget M, Sirigu A (2009) A parietal-premotor network for movement intention and motor awareness. Trends Cogn Sci 13:411–419PubMedCrossRef
go back to reference Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813PubMedCrossRef Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C, Sirigu A (2009) Movement intention after parietal cortex stimulation in humans. Science 324:811–813PubMedCrossRef
go back to reference Gomes G (1998) The timing of conscious experience: a critical review and reinterpretation of Libet’s research. Conscious Cogn 7:559–595PubMedCrossRef Gomes G (1998) The timing of conscious experience: a critical review and reinterpretation of Libet’s research. Conscious Cogn 7:559–595PubMedCrossRef
go back to reference Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484PubMedCrossRef Gratton G, Coles MGH, Donchin E (1983) A new method for off-line removal of ocular artifact. Electroencephalogr Clin Neurophysiol 55:468–484PubMedCrossRef
go back to reference Griffin IC, Nobre AC (2003) Orienting attention to locations in internal representations. J Cogn Neurosci 15:1176–1194PubMedCrossRef Griffin IC, Nobre AC (2003) Orienting attention to locations in internal representations. J Cogn Neurosci 15:1176–1194PubMedCrossRef
go back to reference Guggisberg AG, Dalal SS, Schnider A, Nagarajana SS (2011) The neural basis of event-time introspection. Conscious Cogn 20:1899–1915PubMedCrossRef Guggisberg AG, Dalal SS, Schnider A, Nagarajana SS (2011) The neural basis of event-time introspection. Conscious Cogn 20:1899–1915PubMedCrossRef
go back to reference Haggard P, Eimer M (1999) On the relation between brain potentials and the awareness of voluntary movements. Exp Brain Res 126:128–133PubMedCrossRef Haggard P, Eimer M (1999) On the relation between brain potentials and the awareness of voluntary movements. Exp Brain Res 126:128–133PubMedCrossRef
go back to reference Haggard P, Clark S, Kalogeras J (2002) Voluntary action and conscious awareness. Nat Neurosci 5:382–385PubMedCrossRef Haggard P, Clark S, Kalogeras J (2002) Voluntary action and conscious awareness. Nat Neurosci 5:382–385PubMedCrossRef
go back to reference Hallett M (2007) Volitional control of movement: the physiology of free will. Clin Neurophysiol 118:1179–1192PubMedCrossRef Hallett M (2007) Volitional control of movement: the physiology of free will. Clin Neurophysiol 118:1179–1192PubMedCrossRef
go back to reference Jasper HH (1958) Report of committee on methods of clinical examination in electroencephalography. Electroencephalogr Clin Neurophysiol 10:370–375CrossRef Jasper HH (1958) Report of committee on methods of clinical examination in electroencephalography. Electroencephalogr Clin Neurophysiol 10:370–375CrossRef
go back to reference Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341PubMedCrossRef Kastner S, Ungerleider LG (2000) Mechanisms of visual attention in the human cortex. Annu Rev Neurosci 23:315–341PubMedCrossRef
go back to reference Keller I, Heckhausen B (1990) Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control. Electroencephalogr Clin Neurophysiol 76:351–361PubMedCrossRef Keller I, Heckhausen B (1990) Readiness potentials preceding spontaneous motor acts: voluntary vs. involuntary control. Electroencephalogr Clin Neurophysiol 76:351–361PubMedCrossRef
go back to reference Keller PE, Wascher E, Prinz W, Waszak F, Koch I, Rosenbaum DA (2006) Differences between intention-based and stimulus-based actions. J Psychophysiol 20:9–20CrossRef Keller PE, Wascher E, Prinz W, Waszak F, Koch I, Rosenbaum DA (2006) Differences between intention-based and stimulus-based actions. J Psychophysiol 20:9–20CrossRef
go back to reference 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 86:252–258PubMedCrossRef 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 86:252–258PubMedCrossRef
go back to reference 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 284:1–17PubMedCrossRef 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 284:1–17PubMedCrossRef
go back to reference Krieghoff V, Waszak F, Prinz W, Brass M (2011) Neural and behavioral correlates of intentional actions. Neuropsychologia 49:767–776PubMedCrossRef Krieghoff V, Waszak F, Prinz W, Brass M (2011) Neural and behavioral correlates of intentional actions. Neuropsychologia 49:767–776PubMedCrossRef
go back to reference Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90PubMedCrossRef Lau HC, Rogers RD, Passingham RE (2007) Manipulating the experienced onset of intention after action execution. J Cogn Neurosci 19:81–90PubMedCrossRef
go back to reference Law SK, Rohrbaugh JW, Adams CM, Eckardt MJ (1993) Improving spatial and temporal resolution in evoked EEG responses using surface Laplacians. Electroencephal Clin Neurophysiol 88:309–322CrossRef Law SK, Rohrbaugh JW, Adams CM, Eckardt MJ (1993) Improving spatial and temporal resolution in evoked EEG responses using surface Laplacians. Electroencephal Clin Neurophysiol 88:309–322CrossRef
go back to reference Libet B, Wright EW, Gleason CA (1982) Readiness-potentials preceding unrestricted ‘spontaneous’ vs. pre-planned voluntary acts. Electroenceph Clin Neurophysiol 54:322–335 Libet B, Wright EW, Gleason CA (1982) Readiness-potentials preceding unrestricted ‘spontaneous’ vs. pre-planned voluntary acts. Electroenceph Clin Neurophysiol 54:322–335
go back to reference 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 106:623–642PubMedCrossRef 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 106:623–642PubMedCrossRef
go back to reference 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 125:271–280PubMedCrossRef 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 125:271–280PubMedCrossRef
go back to reference Matsuhashi M, Hallett M (2008) The timing of the conscious intention to move. Eur J Neurosci 28:2344–2351PubMedCrossRef Matsuhashi M, Hallett M (2008) The timing of the conscious intention to move. Eur J Neurosci 28:2344–2351PubMedCrossRef
go back to reference 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 22:103–109PubMedCrossRef 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 22:103–109PubMedCrossRef
go back to reference Nunez PL (2000) Toward a quantitative description of large scale neocortical dynamic function and EEG. Behav Brain Sci 23:371–398PubMedCrossRef Nunez PL (2000) Toward a quantitative description of large scale neocortical dynamic function and EEG. Behav Brain Sci 23:371–398PubMedCrossRef
go back to reference Nunez PL, Srinivasan R (2005) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, New York Nunez PL, Srinivasan R (2005) Electric fields of the brain: the neurophysics of EEG, 2nd edn. Oxford University Press, New York
go back to reference Perrin F, Pernier J, Bertrand D, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184–187PubMedCrossRef Perrin F, Pernier J, Bertrand D, Echallier JF (1989) Spherical splines for scalp potential and current density mapping. Electroencephalogr Clin Neurophysiol 72:184–187PubMedCrossRef
go back to reference Pockett S, Miller A (2007) The rotating spot method of timing subjective events. Conscious Cogn 16:241–254PubMedCrossRef Pockett S, Miller A (2007) The rotating spot method of timing subjective events. Conscious Cogn 16:241–254PubMedCrossRef
go back to reference Rigoni D, Brass M, Sartori G (2010) Post-action determinants of the reported time of conscious intentions. Front Hum Neurosci 4:38PubMed Rigoni D, Brass M, Sartori G (2010) Post-action determinants of the reported time of conscious intentions. Front Hum Neurosci 4:38PubMed
go back to reference 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 22:613–618PubMedCrossRef 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 22:613–618PubMedCrossRef
go back to reference Roskies AL (2010) How does neuroscience affect our conception of volition? Annu Rev Neurosci 33:109–130PubMedCrossRef Roskies AL (2010) How does neuroscience affect our conception of volition? Annu Rev Neurosci 33:109–130PubMedCrossRef
go back to reference 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 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
go back to reference Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356PubMedCrossRef Shibasaki H, Hallett M (2006) What is the Bereitschaftspotential? Clin Neurophysiol 117:2341–2356PubMedCrossRef
go back to reference Shibasaki H, Barrett G, Halliday H, Halliday AM (1980) Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol 49:213–226PubMedCrossRef Shibasaki H, Barrett G, Halliday H, Halliday AM (1980) Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol 49:213–226PubMedCrossRef
go back to reference 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 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
go back to reference Staude G, Flachenecker C, Daumer M, Wolf W (2001) Onset detection in surface electromyographic signals: a systematic comparison of methods. J Appl Sign Process 2:67–81CrossRef Staude G, Flachenecker C, Daumer M, Wolf W (2001) Onset detection in surface electromyographic signals: a systematic comparison of methods. J Appl Sign Process 2:67–81CrossRef
go back to reference Steinmetz H, Fürst G, Meyer BH (1989) Craniocerebral topography within the international 10–20 system. Electroencephalogr Clin Neurophysiol 72:499–506PubMedCrossRef Steinmetz H, Fürst G, Meyer BH (1989) Craniocerebral topography within the international 10–20 system. Electroencephalogr Clin Neurophysiol 72:499–506PubMedCrossRef
go back to reference Taylor M (1978) Bereitschaftspotential during the acquisition of a skilled motor task. Electroencephalogr Clin Neurophysiol 45:568–576PubMedCrossRef Taylor M (1978) Bereitschaftspotential during the acquisition of a skilled motor task. Electroencephalogr Clin Neurophysiol 45:568–576PubMedCrossRef
go back to reference Trevena J, Miller J (2002) Cortical movement preparation before and after a conscious decision to move. Conscious Cogn 11:162–190PubMedCrossRef Trevena J, Miller J (2002) Cortical movement preparation before and after a conscious decision to move. Conscious Cogn 11:162–190PubMedCrossRef
go back to reference Trevena J, Miller J (2010) Brain preparation before a voluntary action: evidence against unconscious movement initiation. Conscious Cogn 19:447–456PubMedCrossRef Trevena J, Miller J (2010) Brain preparation before a voluntary action: evidence against unconscious movement initiation. Conscious Cogn 19:447–456PubMedCrossRef
go back to reference Van Boxtel GJM, Geraats LHD, Van den Berg-Lessen MMC, Brunia CHM (1993) Detection of EMG onset in ERP research. Psychophysiology 30:405–412PubMedCrossRef Van Boxtel GJM, Geraats LHD, Van den Berg-Lessen MMC, Brunia CHM (1993) Detection of EMG onset in ERP research. Psychophysiology 30:405–412PubMedCrossRef
go back to reference 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 106:339–350PubMedCrossRef 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 106:339–350PubMedCrossRef
go back to reference 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 40:796–805PubMedCrossRef 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 40:796–805PubMedCrossRef
go back to reference 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 162:346–356PubMedCrossRef 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 162:346–356PubMedCrossRef
Metadata
Title
Top-down modulation of brain activity underlying intentional action and its relationship with awareness of intention: an ERP/Laplacian analysis
Authors
Davide Rigoni
Marcel Brass
Clémence Roger
Franck Vidal
Giuseppe Sartori
Publication date
01-09-2013
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 3/2013
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-013-3400-0

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