Abstract
A central question in the study of human behavior is the origin of willed action. EEG recordings of surface brain activity from human subjects performing a self-initiated movement show that the subjective experience of wanting to move follows, rather than precedes, the 'readiness potential'—an electrophysiological mark of motor preparation. This raises the issue of how conscious experience of willed action is generated. Here we show that patients with parietal lesions can report when they started moving, but not when they first became aware of their intention to move. This stands in contrast with the performance of cerebellar patients who behaved as normal subjects. We thus propose that when a movement is planned, activity in the parietal cortex, as part of a cortico-cortical sensorimotor processing loop, generates a predictive internal model of the upcoming movement. This model might form the neural correlate of motor awareness.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).
Wolpert, D.M., Ghahramani, Z. & Jordan, M.I. An internal model for sensorimotor integration. Science 269, 1880–1882 (1995).
Blakemore, S.J., Wolpert, D.M. & Frith, C.D. Abnormalities in the awareness of action. Trends Cogn. Sci. 6, 237–242 (2002).
Wolpert, D.M. & Ghahramani, Z. Computational principles of movement neuroscience. Nat. Neurosci. 3, 1212–1217 (2000).
Sirigu, A. et al. The mental representation of hand movements after parietal cortex damage. Science 273, 1564–1568 (1996).
Desmurget, M. & Grafton, S. Forward modeling allows feedback control for fast reaching movements. Trends Cogn. Sci. 4, 423 (2000).
Blakemore, S.J., Frith, C.D. & Wolpert, D.M. The cerebellum is involved in predicting the sensory consequences of action. Neuroreport 12, 1879–1884 (2001).
Flanagan, J.R. & Wing, A.M. The role of internal models in motion planning and control: evidence from grip force adjustments during movements of hand-held loads. J. Neurosci. 17, 1519–1528 (1997).
Babin-Rattè, S., Sirigu, A., Gilles, M. & Wing, A. Impaired anticipatory finger grip-force adjustments in a case of cerebellar degeneration. Exp. Brain Res. 128, 81–85 (1999).
Libet, B., Gleason, C.A., Wright, E.W. & Pearl, D.K. 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 (1983).
Libet, B. Unconscious cerebral initiative and the role of conscious will in voluntary action. Behav. Brain Sci. 8, 529–566 (1985).
Kornhuber, H.H. & Deecke, L. Hirnpotentialänderungen bei Willkürbewegungen und passiven Bewegungen des Menschen: Bereitschaftspotential und reafferente Potentiale. Pflügers Arch. ges. Physiol. 284, 1–17 (1965).
Haggard, P., Clark, S. & Kalogeras, J. Voluntary action and conscious awareness. Nat. Neurosci. 5, 382–385 (2002).
Blakemore, S.J. & Sirigu, A. Action prediction in the cerebellum and in the parietal lobe. Exp. Brain Res. (in press).
Leiguarda, R.C. & Marsden, C.D. Limb apraxias: higher-order disorders of sensorimotor integration. Brain 123, 860–879 (2000).
Shallice, T. & Burgess, P. Deficits in strategy application following frontal lobe damage in man. Brain 114, 727–741 (1991).
Frith, C.D., Blakemore, S.J. & Wolpert, D.M. Abnormalities in the awareness and control of action. Philos. Trans. R. Soc. Lond. B Biol. Sci. 29, 1771–1788 (2000).
Buxbaum. L.J., Sirigu, A., Schwartz, M.F. & Klatzky, R. Cognitive representations of hand posture in ideomotor apraxia. Neuropsychologia 41, 1091–1113 (2003).
Sirigu, A., Daprati, E., Pradat-Diehl, P., Franck, N. & Jeannerod, M. Perception of self-generated movement following left parietal lesion. Brain 122, 1867–1874 (1999).
Weinstein, E.A. & Kahn, R. Denial of Illness: Symbolic and Physiological Aspects (Charles C. Thomas, Springfield, Massachusetts, 1955).
Wolpert, D.M., Ghahramani, Z. & Flanagan, J.R. Perspectives and problems in motor learning. Trends Cogn. Sci. 1, 487–494 (2001).
Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).
Bertrand, O., Perrin, F. & Pernier, J. A theoretical justification of the average reference in topographic evoked potential studies. Electroencephalogr. Clin. Neurophysiol. 62, 462–464 (1985).
McCallum, W.C. Potentials related to expectancy, preparation and motor activity. in Human Event-Related Potentials (ed., Picton, T.W.) 427–534 (Elsevier, Amsterdam, 1988).
Acknowledgements
The authors wish to thank J.R. Duhamel for helpful discussion on a first draft, L. Granjon and B. Messaoudi for assistance during EEG and EMG recording, and A. Cheylus and M. Thevenet for help analyzing EEG data and doing lesion reconstruction. This research was supported by Centre National de la Recherche Scientifique (CNRS).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Fig. 1
Event-related potentials (ERPs) recorded during the control condition (beep). Black line: ERP grand average for normal controls (N = 5); Colored lines: ERPs for each parietal patient. (N= 4). Signal was averaged over beep-locked epochs (from -200 ms to +1000 ms with respect to beep occurrence). Average reference was applied. The first 200 ms of each epoch were used for baseline correction. As shown in the plot, the main components of this stimulus-related activity, namely P100, N200 and P300 are similar in both normal controls and parietal patients. It is important to note that P300 is a late component related to the cognitive processing of the stimulus. A statistical comparison between the two groups for P300 amplitude showed no differences (mean controls 4.421 SD 2.452, mean parietal 3.396 SD 3.099, Mann-Whitney U Test for P300: U= 6.0 Z= 0.9798 P = 0.3272). (JPG 30 kb)
Supplementary Fig. 2
Methods for computing the onset of the RP. We defined the onset of the RP as follows. First, we manually selected an interval of interest that we estimated contained the RP (delimited by the two vertical orange lines). We then computed a linear regression of the data within this interval (orange curves). Parallel lines bounding the minimum and maximum deviation of the RP from the regression line were traced above and below it. A new interval was then defined by extending these lines to include all of the RP variation contained within these bounds. The RP onset was set at the point within this interval at which the value of the RP is at its lowest (i.e, the most positive potential). (JPG 24 kb)
Supplementary Fig. 3
Distribution of the responses given by each subject for the three groups across the three experimental conditions (M-time, W--time, S-time). X-axis: time scale, referred to the clock's face; Y-axis: number of responses given by the subject. (a) controls subjects (CTR 1-5), (b) cerebellar patients (CER 1-5), (c) parietal patietns (PAR 1-5). (PDF 66 kb)
Supplementary Fig. 4
RP controlateral to the responding hand for each parietal patient for M and W condition. (JPG 31 kb)
Rights and permissions
About this article
Cite this article
Sirigu, A., Daprati, E., Ciancia, S. et al. Altered awareness of voluntary action after damage to the parietal cortex. Nat Neurosci 7, 80–84 (2004). https://doi.org/10.1038/nn1160
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1160
This article is cited by
-
Manipulations of Libet clock parameters affect intention timing awareness
Scientific Reports (2022)
-
Neurons as will and representation
Nature Reviews Neuroscience (2022)
-
Impulsivity traits and awareness of motor intention in Parkinson’s disease: a proof-of-concept study
Neurological Sciences (2022)
-
Alien limb phenomenon following posterior cerebral artery stroke: a distinct clinical entity
Journal of Neurology (2020)
-
Twin Loss in the Uterus: Neurodevelopmental Impairment and Reduced Resilience?
Activitas Nervosa Superior (2019)