How can quasi-movements be useful in the examination of voluntary movements? An external perspective integrating neuroscience, psychology, and philosophy

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In 2008, V. Nikulin et al. [1] identified quasi-movements (QM), a type of motor task relying on voluntary movements. QM become noticeable when a person reduces a movement to the point where its associated muscle activity is undetectable through electromyography (EMG) signals. Like overt movements (OM) and kinesthetic motor imagery (imagined movements, IM), QM prompt event-related desynchronization (ERD) of the sensorimotor rhythms of the electroencephalogram (EEG). Drawing upon M. Jeannerod’s [2] claim concerning the existent line of motor system states between OM and IM, Nikulin et al. postulated that QM could fall under a classification of actions in the intermediate section of said range. Notwithstanding, their findings indicate that, as the magnitude of motion dwindles, QM will continue to manifest an agent’s inclination towards executing a physical action. How does the difference in intention relate to the range of possible motor system states across tasks?

In this study, we evaluated the continuum hypothesis based on QM’s intermediate position between physical and mental actions. We developed two versions of this hypothesis. One pertains to the brain mechanisms responsible for executing motor tasks and predicting their sensory outcomes. According to this hypothesis, the operation of these mechanisms continuously shifts between full-fledged OM and IM. Another version of the hypothesis posits the agent’s awareness [3] of action and proposes a continuum of the agent’s mental states ranging from OM to IM. The second version of the hypothesis suggests that the agent perceives certain actions situated between OM and IM (such as QM) as intermediate ones.

If the first version of the continuum hypothesis is correct, a correlation between ERD power and residual EMG in QM would have been expected. This assumption was made based on the realization of the continuum hypothesis. In the case of OM, high muscle activity and desynchronization of the μ-rhythm occur, whereas in the case of IM, there is a significantly lower ERD with almost complete absence of muscle activity. Since muscle tension is a direct result of motor system function, variations in the power of sensorimotor rhythms within a certain range may regulate EMG amplitude. In order to examine the second version of the continuum hypothesis, we have opted to survey participants to gain insight into how individuals subjectively differentiate between QM and OM in addition to IM when viewed from a first-person perspective.

Twenty-three healthy participants took part in our study. The motor tasks in our experiment were based on the thumb abduction method used in Nikulin et al.’s study. This method involves tensing the m. abductor pollicis brevis muscle, enabling accurate measurement of muscle activity. The experiment was conducted over two days, with participants receiving training on the first day for performing thumb abduction, QM, and kinesthetic motor imagery. On the second day, participants replicated their learned skills under three conditions, each corresponding to a different motor task. They rhythmically performed OM, QM, or IM following rhythms consisting of three tones in each condition. To facilitate EEG analysis, the motor tasks were compared to a visual attention task that required participants to count the elements in a picture. On the second day, the participants’ EMG and 128-channel EEG were recorded.

Using more sensitive processing methods than in previous studies [1, 4, 5], we analyzed the disparity between ERD in QM and IM and explored the correlation between EMG parameters and ERD power in QM. Furthermore, we administered a survey to the participants, focusing on their perception of motion in QM and its realism. The respondents provided affirmative or negative responses. We asked participants to provide in-depth reports on the subjective distinctions between QM and OM/IM. Our aim was to examine whether judgments about QM were impacted by residual EMG by comparing these responses with EMG data.

The average EMG values obtained in both QM and IM were comparable to those found by Nikulin et al. Nevertheless, a thorough examination of the EMG data demonstrated heightened peak muscle activity in QM trials. While the contralateral component of the ERD μ-rhythm was independent of the EMG amplitude, it exhibited greater strength in QM as opposed to IM. This result indicates that QM strictly defined and those accompanied by increased muscle activity have a stable pattern of motor system activity that differs significantly from that of IM. Therefore, QM is more likely to constitute a distinct motor phenomenon.

In addition to EEG analysis, we examined subjective reports from participants. We categorized the free-form reports into common descriptors of variations in motor tasks and examined the connection between the descriptors, question responses, and the proportion of trials with elevated EMG in the QM condition. There was no correlation between the proportion of trials with elevated EMG and the participants’ reports on the feeling of movement or the perceived reality of QM. In addition, the descriptors distinguishing QM from IM were not influenced by the residual EMG. Analysis of the free-form reports revealed that participants had comparable intentions in both the OM and QM conditions, which differed from those in the IM condition. The intention to execute a movement in the QM condition correlated with References to “sending a command” to the muscles. Additionally, the perceived reality of QM correlated with mentions of muscle tension during QM, indicating sensory feedback.

The obtained results are not well-matched with either version of the continuum hypothesis. The lack of correlation between EMG and the contralateral element of μ-rhythm desynchronization suggests that the simplest realization of the first version is incorrect. Although QM acts as an intermediate between OM and IM, and EEG presents it as a steady independent phenomenon instead of being part of a continuous range of actions. Subjectively, QM is experienced as an OM with insufficient feedback. This reduces the agent’s confidence regarding the movement’s reality. The agent’s awareness when performing QM and IM differs in quality as they are distinct actions, despite potential imagined feedback in QM. Our study has some limitations, specifically regarding the range of actions between overt and imagined movements, which may not necessarily involve QM. The states within the continuum may possess a complexity greater than the previously assumed arrangement. Another limitation is associated with the experiment’s relatively small sample size. It would be advantageous to use a larger sample size to gain better insights into studying QM.

全文:

In 2008, V. Nikulin et al. [1] identified quasi-movements (QM), a type of motor task relying on voluntary movements. QM become noticeable when a person reduces a movement to the point where its associated muscle activity is undetectable through electromyography (EMG) signals. Like overt movements (OM) and kinesthetic motor imagery (imagined movements, IM), QM prompt event-related desynchronization (ERD) of the sensorimotor rhythms of the electroencephalogram (EEG). Drawing upon M. Jeannerod’s [2] claim concerning the existent line of motor system states between OM and IM, Nikulin et al. postulated that QM could fall under a classification of actions in the intermediate section of said range. Notwithstanding, their findings indicate that, as the magnitude of motion dwindles, QM will continue to manifest an agent’s inclination towards executing a physical action. How does the difference in intention relate to the range of possible motor system states across tasks?

In this study, we evaluated the continuum hypothesis based on QM’s intermediate position between physical and mental actions. We developed two versions of this hypothesis. One pertains to the brain mechanisms responsible for executing motor tasks and predicting their sensory outcomes. According to this hypothesis, the operation of these mechanisms continuously shifts between full-fledged OM and IM. Another version of the hypothesis posits the agent’s awareness [3] of action and proposes a continuum of the agent’s mental states ranging from OM to IM. The second version of the hypothesis suggests that the agent perceives certain actions situated between OM and IM (such as QM) as intermediate ones.

If the first version of the continuum hypothesis is correct, a correlation between ERD power and residual EMG in QM would have been expected. This assumption was made based on the realization of the continuum hypothesis. In the case of OM, high muscle activity and desynchronization of the μ-rhythm occur, whereas in the case of IM, there is a significantly lower ERD with almost complete absence of muscle activity. Since muscle tension is a direct result of motor system function, variations in the power of sensorimotor rhythms within a certain range may regulate EMG amplitude. In order to examine the second version of the continuum hypothesis, we have opted to survey participants to gain insight into how individuals subjectively differentiate between QM and OM in addition to IM when viewed from a first-person perspective.

Twenty-three healthy participants took part in our study. The motor tasks in our experiment were based on the thumb abduction method used in Nikulin et al.’s study. This method involves tensing the m. abductor pollicis brevis muscle, enabling accurate measurement of muscle activity. The experiment was conducted over two days, with participants receiving training on the first day for performing thumb abduction, QM, and kinesthetic motor imagery. On the second day, participants replicated their learned skills under three conditions, each corresponding to a different motor task. They rhythmically performed OM, QM, or IM following rhythms consisting of three tones in each condition. To facilitate EEG analysis, the motor tasks were compared to a visual attention task that required participants to count the elements in a picture. On the second day, the participants’ EMG and 128-channel EEG were recorded.

Using more sensitive processing methods than in previous studies [1, 4, 5], we analyzed the disparity between ERD in QM and IM and explored the correlation between EMG parameters and ERD power in QM. Furthermore, we administered a survey to the participants, focusing on their perception of motion in QM and its realism. The respondents provided affirmative or negative responses. We asked participants to provide in-depth reports on the subjective distinctions between QM and OM/IM. Our aim was to examine whether judgments about QM were impacted by residual EMG by comparing these responses with EMG data.

The average EMG values obtained in both QM and IM were comparable to those found by Nikulin et al. Nevertheless, a thorough examination of the EMG data demonstrated heightened peak muscle activity in QM trials. While the contralateral component of the ERD μ-rhythm was independent of the EMG amplitude, it exhibited greater strength in QM as opposed to IM. This result indicates that QM strictly defined and those accompanied by increased muscle activity have a stable pattern of motor system activity that differs significantly from that of IM. Therefore, QM is more likely to constitute a distinct motor phenomenon.

In addition to EEG analysis, we examined subjective reports from participants. We categorized the free-form reports into common descriptors of variations in motor tasks and examined the connection between the descriptors, question responses, and the proportion of trials with elevated EMG in the QM condition. There was no correlation between the proportion of trials with elevated EMG and the participants’ reports on the feeling of movement or the perceived reality of QM. In addition, the descriptors distinguishing QM from IM were not influenced by the residual EMG. Analysis of the free-form reports revealed that participants had comparable intentions in both the OM and QM conditions, which differed from those in the IM condition. The intention to execute a movement in the QM condition correlated with References to “sending a command” to the muscles. Additionally, the perceived reality of QM correlated with mentions of muscle tension during QM, indicating sensory feedback.

The obtained results are not well-matched with either version of the continuum hypothesis. The lack of correlation between EMG and the contralateral element of μ-rhythm desynchronization suggests that the simplest realization of the first version is incorrect. Although QM acts as an intermediate between OM and IM, and EEG presents it as a steady independent phenomenon instead of being part of a continuous range of actions. Subjectively, QM is experienced as an OM with insufficient feedback. This reduces the agent’s confidence regarding the movement’s reality. The agent’s awareness when performing QM and IM differs in quality as they are distinct actions, despite potential imagined feedback in QM. Our study has some limitations, specifically regarding the range of actions between overt and imagined movements, which may not necessarily involve QM. The states within the continuum may possess a complexity greater than the previously assumed arrangement. Another limitation is associated with the experiment’s relatively small sample size. It would be advantageous to use a larger sample size to gain better insights into studying QM.

ADDITIONAL INFORMATION

Funding sources. This research was funded by the Russian Science Foundation, grant No. 22-29-01361 (materials and investigation) and grant No. 22-19-00528 (data processing and theoretical analysis).

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作者简介

A. Yashin

Moscow State University of Psychology and Education; Lomonosov Moscow State University

编辑信件的主要联系方式.
Email: yashinart1996@gmail.com
俄罗斯联邦, Moscow; Moscow

A. Vasilyev

Moscow State University of Psychology and Education; Lomonosov Moscow State University

Email: yashinart1996@gmail.com
俄罗斯联邦, Moscow; Moscow

S. Shishkin

Moscow State University of Psychology and Education

Email: yashinart1996@gmail.com
俄罗斯联邦, Moscow

参考

  1. Nikulin VV, Hohlefeld FU, Jacobs AM, Curio G. Quasi-movements: A novel motor-cognitive phenomenon. Neuropsychologia. 2008;46(2):727–742. doi: 10.1016/j.neuropsychologia.2007.10.008
  2. Jeannerod M. The representing brain: Neural correlates of motor intention and imagery. Behavioral and Brain Sciences. 1994;17(2):187–202. doi: 10.1017/S0140525X00034026
  3. Mylopoulos MI, Shepherd J. The experience of agency. In: Kriegel U, editor. The Oxford Handbook of the Philosophy of Consciousness 2020. Oxford: Oxford University Press; 2020:164–187. doi: 10.1093/oxfordhb/9780198749677.013.8
  4. Higashi H, Rutkowski TM, Washizawa Y, et al. Imagery Movement Paradigm User Adaptation Improvement with Quasi-movements Phenomenon. In: Wang R, Gu F, editors. Advances in Cognitive Neurodynamics (II) 2011. Berlin: Springer; 2011:677–681. doi: 10.1007/978-90-481-9695-1_101
  5. Zich C, Debener S, De Vos M, et al. Lateralization patterns of covert but not overt movements change with age: An EEG neurofeedback study. NeuroImage. 2015;116:80–91. doi: 10.1016/j.neuroimage.2015.05.009

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