Temporal dynamics of the mirror neurons effect and its stimuli dependent modulation: TMS study

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Abstract

The study of mirror neurons (MN) has made significant progress since human studies commenced. However, when using transcranial magnetic stimulation (TMS), there are inconsistencies in the literature regarding stimulus presentation, duration of presentation, and timing of TMS pulses.

The study assessed the effects of stimuli presentations, using both pictures and videos of hand movements. To accomplish this, single-pulse TMS was applied to the dominant primary motor cortex (M1) during varying time frames (0, 320, 640 ms). Motor evoked potentials were then recorded from the FDI (index finger) and ADM (little finger) muscles of 29 healthy participants via adhesive electrodes. Subjects’ hands were positioned perpendicular to each other, and visual stimuli were presented under three varying conditions. The TMS coil was accurately repositioned using an Axilum Cobot robotic arm and navigation stimulation system to maintain consistency throughout the experiment.

The aim of this study is to provide a comprehensive analysis of stimulus presentation and stimulation timeframes to achieve optimal settings. This paper describes the two most commonly used stimulus modalities, namely, picture and video [1–4], and the frequently employed timeframes for TMS: from movement initiation (picture and video condition) to offset (post-video condition), with different timings (0, 320, and 640 ms) [1, 2, 5]. Notably, the stimulation at the offset of the movement is a novel concept in literature. We conducted three distinct three-way repeated measures ANOVAs employing independent variables. The collected data indicate that the two types of stimulation during the onset of movement, i.e., photograph and video, display varying changes over time. At 320 ms, MEPs increase for the related muscles while nonrelated muscles exhibit inhibitory effects at 640 ms. In the condition of stimulation during movement offset (post-video), this double dissociation is present across all stimulation time frames. Hence, the majority of mirror response can be attributed to inhibition of nonrelated muscles. This study displays the temporal progression of the mirror effect and its impact on both related and unrelated muscles throughout time.

The obtained data illuminates unresolved inquiries in human mirror neuron research and details the impacts of diverse stimuli presentations and TMS stimulation durations. With this information, an ideal protocol can be established to examine the human mirror neuron system tailored to specific research needs. Furthermore, these outcomes can foster the creation of enhanced rehabilitation protocols for patients with movement disorders in clinical settings.

Full Text

The study of mirror neurons (MN) has made significant progress since human studies commenced. However, when using transcranial magnetic stimulation (TMS), there are inconsistencies in the literature regarding stimulus presentation, duration of presentation, and timing of TMS pulses.

The study assessed the effects of stimuli presentations, using both pictures and videos of hand movements. To accomplish this, single-pulse TMS was applied to the dominant primary motor cortex (M1) during varying time frames (0, 320, 640 ms). Motor evoked potentials were then recorded from the FDI (index finger) and ADM (little finger) muscles of 29 healthy participants via adhesive electrodes. Subjects’ hands were positioned perpendicular to each other, and visual stimuli were presented under three varying conditions. The TMS coil was accurately repositioned using an Axilum Cobot robotic arm and navigation stimulation system to maintain consistency throughout the experiment.

The aim of this study is to provide a comprehensive analysis of stimulus presentation and stimulation timeframes to achieve optimal settings. This paper describes the two most commonly used stimulus modalities, namely, picture and video [1–4], and the frequently employed timeframes for TMS: from movement initiation (picture and video condition) to offset (post-video condition), with different timings (0, 320, and 640 ms) [1, 2, 5]. Notably, the stimulation at the offset of the movement is a novel concept in literature. We conducted three distinct three-way repeated measures ANOVAs employing independent variables. The collected data indicate that the two types of stimulation during the onset of movement, i.e., photograph and video, display varying changes over time. At 320 ms, MEPs increase for the related muscles while nonrelated muscles exhibit inhibitory effects at 640 ms. In the condition of stimulation during movement offset (post-video), this double dissociation is present across all stimulation time frames. Hence, the majority of mirror response can be attributed to inhibition of nonrelated muscles. This study displays the temporal progression of the mirror effect and its impact on both related and unrelated muscles throughout time.

The obtained data illuminates unresolved inquiries in human mirror neuron research and details the impacts of diverse stimuli presentations and TMS stimulation durations. With this information, an ideal protocol can be established to examine the human mirror neuron system tailored to specific research needs. Furthermore, these outcomes can foster the creation of enhanced rehabilitation protocols for patients with movement disorders in clinical settings.

ADDITIONAL INFORMATION

Funding sources. The research was conducted using the HSE automated system of non-invasive brain stimulation with the possibility of synchronous registration of brain activity and registration of eye movements, with the financial support of the Ministry of Science and Higher Education of the Russian Federation, grant No. 075-15-2021-673.

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About the authors

C. Nieto Doval

National Research University “Higher School of economics”

Author for correspondence.
Email: carlosnietodoval@gmail.com
Russian Federation, Moscow

A. A. Ragimova

National Research University “Higher School of economics”

Email: carlosnietodoval@gmail.com
Russian Federation, Moscow

M. Feurra

National Research University “Higher School of economics”

Email: carlosnietodoval@gmail.com
Russian Federation, Moscow

References

  1. Barchiesi G, Cattaneo L. Early and late motor responses to action observation. Social cognitive and affective neuroscience. 2013;8(6):711–719. doi: 10.1093/scan/nss049
  2. Catmur C, Walsh V, Heyes C. Sensorimotor Learning Configures the Human Mirror System. Current Biology. 2007;17(17):1527–1531. doi: 10.1016/j.cub.2007.08.006
  3. Errante A, Fogassi L. Activation of cerebellum and basal ganglia during the observation and execution of manipulative actions. Scientific reports. 2020;10(1):12008. doi: 10.1038/s41598-020-68928-w
  4. Received: 15.05.2023 Accepted: 26.11.2023 Published online: 20.01.2024
  5. Taschereau-Dumouchel V, Hétu S, Michon PE, et al. BDNF Val66Met polymorphism influences visuomotor associative learning and the sensitivity to action observation. Scientific reports. 2016;6:34907. doi: 10.1038/srep34907
  6. Catmur C, Walsh V, Heyes C. Associative sequence learning: the role of experience in the development of imitation and the mirror system. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364(1528):2369–2380. doi: 10.1098/rstb.2009.0048

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