Rapid CommunicationIs the movement-evoked potential mandatory for movement execution? A high-resolution EEG study in a deafferented patient
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.
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2012, NeuroImageCitation 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).
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2011, Neurobiology of AgingCitation 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.
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2009, Trends in Cognitive SciencesCitation 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.
Effect of sensory attenuation on cortical movement-related oscillations
2018, Journal of NeurophysiologyMotor unit firing pattern, synchrony and coherence in a deafferented patient
2014, Frontiers in Human Neuroscience