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Altered awareness of voluntary action after damage to the parietal cortex

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.

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Figure 1: Task procedure and EEG recording sites.
Figure 2: Behavioral data.
Figure 3: Samples of EEG recording.
Figure 4: Lesioned cortical region (blue area) common to all five parietal patients.

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References

  1. Kawato, M. Internal models for motor control and trajectory planning. Curr. Opin. Neurobiol. 9, 718–727 (1999).

    Article  CAS  Google Scholar 

  2. Wolpert, D.M., Ghahramani, Z. & Jordan, M.I. An internal model for sensorimotor integration. Science 269, 1880–1882 (1995).

    Article  CAS  Google Scholar 

  3. Blakemore, S.J., Wolpert, D.M. & Frith, C.D. Abnormalities in the awareness of action. Trends Cogn. Sci. 6, 237–242 (2002).

    Article  Google Scholar 

  4. Wolpert, D.M. & Ghahramani, Z. Computational principles of movement neuroscience. Nat. Neurosci. 3, 1212–1217 (2000).

    Article  CAS  Google Scholar 

  5. Sirigu, A. et al. The mental representation of hand movements after parietal cortex damage. Science 273, 1564–1568 (1996).

    Article  CAS  Google Scholar 

  6. Desmurget, M. & Grafton, S. Forward modeling allows feedback control for fast reaching movements. Trends Cogn. Sci. 4, 423 (2000).

    Article  CAS  Google Scholar 

  7. 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).

    Article  CAS  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

  9. 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).

    Article  Google Scholar 

  10. 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).

    Article  Google Scholar 

  11. Libet, B. Unconscious cerebral initiative and the role of conscious will in voluntary action. Behav. Brain Sci. 8, 529–566 (1985).

    Article  Google Scholar 

  12. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  14. Blakemore, S.J. & Sirigu, A. Action prediction in the cerebellum and in the parietal lobe. Exp. Brain Res. (in press).

  15. Leiguarda, R.C. & Marsden, C.D. Limb apraxias: higher-order disorders of sensorimotor integration. Brain 123, 860–879 (2000).

    Article  Google Scholar 

  16. Shallice, T. & Burgess, P. Deficits in strategy application following frontal lobe damage in man. Brain 114, 727–741 (1991).

    Article  Google Scholar 

  17. 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).

    Article  Google Scholar 

  18. Buxbaum. L.J., Sirigu, A., Schwartz, M.F. & Klatzky, R. Cognitive representations of hand posture in ideomotor apraxia. Neuropsychologia 41, 1091–1113 (2003).

    Article  Google Scholar 

  19. 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).

    Article  Google Scholar 

  20. Weinstein, E.A. & Kahn, R. Denial of Illness: Symbolic and Physiological Aspects (Charles C. Thomas, Springfield, Massachusetts, 1955).

    Book  Google Scholar 

  21. Wolpert, D.M., Ghahramani, Z. & Flanagan, J.R. Perspectives and problems in motor learning. Trends Cogn. Sci. 1, 487–494 (2001).

    Article  Google Scholar 

  22. Oldfield, R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9, 97–113 (1971).

    Article  CAS  Google Scholar 

  23. 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).

    Article  CAS  Google Scholar 

  24. 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).

    Google Scholar 

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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).

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Correspondence to Angela Sirigu.

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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)

Supplementary Table 1 (PDF 12 kb)

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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

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