Elsevier

NeuroImage

Volume 31, Issue 2, June 2006, Pages 677-685
NeuroImage

Rapid Communication
Is the movement-evoked potential mandatory for movement execution? A high-resolution EEG study in a deafferented patient

https://doi.org/10.1016/j.neuroimage.2005.12.053Get rights and content

Abstract

During simple self-paced index finger flexion with and without visual feedback of the finger, we compared the movement-evoked potentials of the completely deafferented patient GL with those of 7 age-matched healthy subjects. EEG was recorded from 58 scalp positions, together with the electromyogram (EMG) from the first dorsal interosseous muscle and the movement trace. We analyzed the movement parameters and the contralateral movement-evoked potential and its source. The patient performed the voluntary movements almost as well as the controls in spite of her lack of sensory information from the periphery. In contrast, the movement-evoked potential was observed only in the controls and not in the patient. These findings clearly demonstrate that the movement-evoked potential reflects cutaneous and proprioceptive feedback from the moving part of the body. They also indicate that in absence of sensory peripheral input the motor control switches from an internal “sensory feedback-driven” to a “feedforward” mode. The role of the sensory feedback in updating the internal models and of the movement-evoked potential as a possible cortical correlate of motor awareness is discussed.

Introduction

There is an increasing body of experimental evidence, coming from various approaches, favoring the hypothesis that the cortical activity between 90 and 120 ms after movement onset reflects sensory feedback from the moving part of the body. After the movement onset, an increase in neuronal activity in somatosensory cortex has been recorded in monkeys (Evarts and Fromm, 1977, Wannier et al., 1991) and a negative peak called the “hand somatosensory potential” reported in humans (Neshige et al., 1988). This activity, manifested as movement-evoked potential (MEP), was considered by most of the electrical macropotential studies, including the pioneering work of Kornhuber and Deecke (1965) who introduced the Bereitschaftspotential paradigm (BP) as a typical paradigm to study voluntary movement-related activity, as reflecting proprioceptive input from the periphery (Kristeva et al., 1979, Tarkka and Hallett, 1991, Kornhuber and Deecke, 1965). These EEG studies provided consistent evidence that the topographic distribution of the MEP is characterized by a bipolar pattern with a maximum of negativity over the fronto-central midline and a positivity above the contralateral parietal areas. This pattern is caused by the activation of a network in the contralateral somatosensory area as shown by electric and magnetic source reconstruction (Toro et al., 1993, Ball et al., 1999, Toma et al., 2002, Toma and Hallett, 2003, Kristeva-Feige et al., 1994, Kristeva-Feige et al., 1995, Cheyne and Weinberg, 1989, Kristeva et al., 1991). Further arguments favoring the peripheral origin of the MEP came from its somatotopic organization (Walter et al., 1992) and from the finding that it had a longer latency for toe than for finger movements.

Cheyne et al. (1997) using MEG showed that cooling the subject's arm resulted in delays of about 8 ms in the MEP latency. This delay was attributed to an increase in conduction time in the afferent pathways as confirmed by electrically evoked somatosensory responses and thus, strongly suggested a peripheral origin for the movement-evoked field. In a previous study of ours (Kristeva-Feige et al., 1996), we demonstrated that elimination of cutaneous inputs by anesthetic nerve block modulated the MEP amplitude, suggesting that this potential reflects not only proprioceptive but also cutaneous input from the periphery. This finding was not surprising as Edin and Abbs (1991) and Edin (1992) undoubtedly showed that “cutaneous input from the moving part of the body also plays a specific role in motor control”.

If the MEP reflects somatosensory input from the periphery, one can predict that this component will not be present in deafferented patients. For this purpose, we recorded the movement-related cortical activity and the movement kinematics in the deafferented patient GL and in seven healthy control subjects while they performed self-paced flexion movements of the index finger every 12–24 s (typical Bereitschaftspotential paradigm, Kornhuber and Deecke, 1965). To have a reasonable spatial resolution, we recorded the movement-related activity from 58 scalp positions. In addition, we performed advanced source reconstruction analysis for the deafferented patient and four controls. This analysis which takes into consideration the individual anatomy from the MRI data of the patient and the control subjects successfully defines the spatiotemporal pattern of activation of the motor areas during planning and execution of simple and complex movements (Ball et al., 1999, Kristeva-Feige, 2003).

The second aim of the study was to investigate the contribution made by the visual feedback to cortical activity and motor performance of this simple finger movement. For this purpose, movement-related activity and kinematics were investigated under two experimental conditions: with and without visual feedback of the moving finger.

The study demonstrated that the patient GL did not show any MEP although she performed the simple pulse movements almost as well as the control subjects. The results are discussed within the framework for optimal motor control (Wolpert and Ghahramani, 2000) and awareness of action.

Section snippets

Subjects

The deafferented patient GL, a right-handed 55-year-old woman, participated in the study (for detailed clinical description, cf. Forget and Lamarre (1987) and http://www.deafferented.apinc.org//). After two episodes of polyneuropathy (at the age of 27 and 31), the patient has been suffering from a strong sensory impairment of the whole body up to the nose due to affected large diameter peripheral sensory myelinated fibers. The impairment was documented by sural biopsy. The patient had a total

Movement parameters with and without visual feedback

Representative examples of the goniometric trajectories with and without visual control are displayed in the lower part of Fig. 3, for the patient and four control subjects. The quantitative analysis of the trajectories is shown in Fig. 2 for the patient and all seven subjects.

The upper part of Fig. 2 shows mean amplitude duration and rise time values for each subject and the lower part shows their respective variance. It is obvious that the mean values obtained by the patient fit in the

Movement-evoked potential (MEP) reflects somatosensory input from the periphery

The basic hypothesis tested in this study was that the MEP, i.e. the cortical potential occurring at approximately 90 ms after a voluntary movement, would be absent from a deafferented patient suffering from a large-fiber sensory neuropathy. The present results confirmed this hypothesis as in contrast to the controls, the patient GL did not show any early postmovement MEP (Fig. 3). Thus, this finding provides clear evidence that MEP reflects sensory (cutaneous and proprioceptive) input from the

Acknowledgments

The authors thank J. Paillard for having made possible the experiment with the patient GL, J. Spreer for the MRIs, H. Hampel for experimental help and last but not least GL for her devotion to science. This study was supported by DFG grant KR 1392/7-3.

References (51)

  • R. Kristeva et al.

    Neuromagnetic fields accompanying unilateral and bilateral voluntary movements: topography and analysis of cortical sources

    Electroencephalogr. Clin. Neurophysiol.

    (1991)
  • R. Kristeva-Feige et al.

    Neuromagnetic fields of the brain evoked by voluntary movement and electrical stimulation of the index finger

    Brain Res.

    (1995)
  • R. Kristeva-Feige et al.

    Changes in movement-related brain activity during transient deafferentation: a neuromagnetic study

    Brain Res.

    (1996)
  • S. Makeig et al.

    Mining event-related brain dynamics

    Trends Cogn. Sci.

    (2004)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychology

    (1971)
  • K. Toma et al.

    Generators of movement-related cortical potentials: fMRI-constrained EEG dipole source analysis

    NeuroImage

    (2002)
  • C. Toro et al.

    Source analysis of scalp-recorded movement-related electrical potentials

    Electroencephalogr. Clin. Neurophysiol.

    (1993)
  • H.G. Vaughan et al.

    Cortical motor potential in monkeys before and after upper limb deafferentation

    Exp. Neurol.

    (1970)
  • D.M. Wolpert et al.

    Motor prediction

    Curr. Biol.

    (2001)
  • D. Cheyne et al.

    Neuromagnetic fields accompanying unilateral finger movements: pre-movement and movement-evoked fields

    Exp. Brain Res.

    (1989)
  • J.D. Cole et al.

    Evoked potentials in a subject with a large-fibre sensory neuropathy below the neck

    Can. J. Physiol. Pharmacol.

    (1995)
  • B.B. Edin

    Quantitative analysis of static strain sensitivity in human mechanoreceptors from hairy skin

    J. Neurophysiol.

    (1992)
  • B.B. Edin et al.

    Finger movement responses of cutaneous mechanoreceptors in the dorsal skin of the human hand

    J. Neurophsiol.

    (1991)
  • R. Forget et al.

    Rapid elbow flexion in the absence of proprioceptive and cutaneous feedback

    Hum. Neurobiol.

    (1987)
  • G.H. Golub et al.

    Matrix Computations

    (1989)
  • Cited by (15)

    • Cortical post-movement and sensory processing disentangled by temporary deafferentation

      2012, NeuroImage
      Citation Excerpt :

      The interval for the movement-evoked potential reflecting reafferent somatosensory input (MEP-I, or movement-evoked field I in MEG studies; Cheyne and Weinberg, 1989; Kristeva et al., 1991; Salmelin et al., 1995) was determined at leads CP3, CP4. It incorporated the previously reported latencies: 350–600 ms after the imperative stimulus (stimulus-locked analysis) and 70–170 ms after EMG onset (response-locked analysis) (Botzel et al., 1997; Cheyne and Weinberg, 1989; Gerloff et al., 1998; Kristeva et al., 2006; Nagamine et al., 1994; Neshige et al., 1988; Seiss et al., 2002; Toma et al., 2002). The initial negative motor potential peak (trigger of the cortico-spinal volley; Kristeva et al., 1991; Nagamine et al., 1994; Tarkka and Hallett, 1991a) was determined using automatic peak detection during the time interval 100 ms before the onset of the EMG response and 150 ms thereafter at electrode C3 (for the dominant right hand reaction).

    • Cortical control of unilateral simple movement in healthy aging

      2011, Neurobiology of Aging
      Citation Excerpt :

      SMC activity, also present during early BP (Ikeda et al., 1996) first mainly contralateral and then ipsilateral to movement, become relevant during late preparation, when, through intense interactions with SMA aimed at selecting the appropriate muscles synergies (Wildgruber et al., 1997; Colebatch, 2007), the conscious will to move is transformed into the execution of a certain movement (Shibasaki and Hallett, 2006). Finally, SMC shows the contribution of both motor (Kristeva et al., 2006) and sensory regions during movement-evoked phase (MP1), representing the afferent feedback processing. In the present study, cSMC resulted the most intensely active region during the last two periods.

    • A parietal-premotor network for movement intention and motor awareness

      2009, Trends in Cognitive Sciences
      Citation Excerpt :

      These observations are consistent with clinical reports in deafferented patients. As shown in recent studies, these patients exhibit normal motor awareness, even though they have no perceptual awareness [32–34]. They can report when they are moving and along which trajectory, but cannot detect, for instance, that their hand has been blocked at movement onset.

    View all citing articles on Scopus
    View full text