Yıl: 2023 Cilt: 53 Sayı: 5 Sayfa Aralığı: 1428 - 1437 Metin Dili: İngilizce DOI: 10.55730/1300-0144.5710 İndeks Tarihi: 29-11-2023

Mirror neuron activity depending on the content and stage of the observed action: a TMS study

Öz:
Background/aim: The firing rate of the mirror neuron system in monkeys decreases systematically with more repetitions. The aim of this study is to investigate whether the activity of the mirror neuron system varies based on the observed movement and the contents of the action, as well as whether there is inhibition in the mirror neuron system when humans observe repeated actions. If inhibition is present, the second question of the study is whether it is related to the organization of the observed action. Materials and methods: Fourteen healthy volunteers participated in the study. Transcranial magnetic stimulation was applied to the left primary motor cortex and motor evoked potentials (MEPs) were recorded from the right first dorsal interosseous and abductor pollicis brevis muscles while the participants were watching videos specially prepared for the study. Results: There were no significant changes in MEP amplitudes compared to baseline MEPs while observing aimless action. However, while participants watched the repeated action video, the mean MEP amplitude increased at the beginning of the movement, but neither facilitation nor inhibition was detected when the participants watched the phase of grasping the object of the action compared to the baseline MEP amplitude. On the other hand, while participants were watching different activities, an increased MEP amplitude was ob- served at the beginning of the movement and in the grasping of the object of the action. Additionally, there was no significant reduction in MEP amplitude during any movement stages while observing the repeated action video. Conclusion: The findings of this study suggest that the activation of the mirror neuron system in humans depends on the content and stages of the observed movement. Additionally, there was no inhibition or systematic reduction in MEP amplitudes while watching a repeated action.
Anahtar Kelime: Mirror neuron system transcranial magnetic stimulation motor evoked potential repeated action observation

Belge Türü: Makale Makale Türü: Araştırma Makalesi Erişim Türü: Erişime Açık
  • 1. Di Pellegrino G, Fadiga L, Fogassi L, Gallese V, Rizzolatti G. Understanding motor events: a neurophysiological study. Experimental Brain Research 1992; 91: 176-180. https://doi. org/10.1007/BF00230027
  • 2. Fogassi, L, Gallese, V, Fadiga, L, Rizzolatti, G. Neurons responding to the sight of goal directed hand/arm actions in the parietal area PF (7b) of the macaque monkey. In: 28th Annual Meeting of Society for Neuroscience; Los Angeles, CA, USA; 1998. p. 257.
  • 3. Rizzolatti G, Fadiga L, Matelli M, Bettinardi V, Paulesu E et al. Localization of grasp representations in humans by PET: 1. Observation versus execution. Experimental Brain Research 1996; 111: 246-252. https://doi.org/10.1007/BF00227301
  • 4. Decety J, Grezes J, Costes N, Perani D, Jeannerod M et al. Brain activity during observation of actions. Influence of action content and subject’s strategy. Brain 1997; 120: 1763-1777. https://doi.org/10.1093/brain/120.10.1763
  • 5. Kraskov A, Philipp R, Waldert S, Vigneswaran G, Quallo MM et al. Corticospinal mirror neurons. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 2014; 369 (1644): 20130174. https://doi.org/10.1098/rstb.2013.0174
  • 6. Umilta MA, Kohler E, Gallese V, Fogassi L, Fadiga L et al. I know what you are doing. A neurophysiological study. Neuron 2001; 31: 155-165. https://doi.org/10.1016/s0896-6273(01)00337-3
  • 7. Kohler E, Keysers C, Umiltà MA, Fogassi L, Gallese V et al. Hearing sounds, understanding actions: action representation in mirror neurons. Science 2002; 297: 846-848. https://doi. org/10.1126/science.1070311
  • 8. Rizzolatti G, Fogassi L, Gallese V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Reviews Neuroscience 2001; 2: 661-670. https:// doi.org/10.1038/35090060
  • 9. Buccino G, Binkofski F, Fink G, Fadiga L, Fogassi L et al. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. European Journal of Neuroscience 2001; 13: 400-404. https://doi.org/10.1111/ j.1460-9568.2001.01385.x
  • 10. Iacoboni M, Woods RP, Brass M, Bekkering H, Mazziotta JC et al. Cortical mechanisms of human imitation. Science 1999; 286: 2526-2528. https://doi.org/10.1126/science.286.5449.2526
  • 11. Frey SH, Vinton D, Norlund R, Grafton ST. Cortical topography of human anterior intraparietal cortex active during visually guided grasping. Cognitive Brain Research 2005; 23: 397-405. https://doi.org/10.1016/j.cogbrainres.2004.11.010
  • 12. Grezes J, Decety J. Functional anatomy of execution, mental simulation, observation, and verb generation of actions: a meta- analysis. Human Brain Mapping 2001; 12: 1-19. https://doi. org/10.1002/1097-0193(200101)12:1<1::aid-hbm10>3.0.co;2-v
  • 13. Rizzolatti G, Craighero L. The mirror-neuron system. Annual Review of Neuroscience 2004; 27: 169-192. https://doi. org/10.1146/annurev.neuro.27.070203.144230
  • 14. Miller EK, Gochin P, Gross CG. Habituation-like decrease in the responses of neurons in inferior temporal cortex of the macaque. Visual Neuroscience 1991; 7: 357-362. https://doi. org/10.1017/s0952523800004843
  • 15. Naccache L, Dehaene S. The priming method: imaging unconscious repetition priming reveals an abstract representation of number in the parietal lobes. Cerebral Cortex 2001; 11: 966-974. https://doi.org/10.1093/cercor/11.10.966
  • 16. Grill-Spector K, Malach R. fMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychologica 2001; 107: 293-321. https://doi.org/10.1016/ s0001-6918(01)00019-1
  • 17. Thompson-Schill SL, D’Esposito M, Kan IP. Effects of repetition and competition on activity in left prefrontal cortex during word generation. Neuron 1999; 23: 513-522. https://doi.org/10.1016/ s0896-6273(00)80804-1
  • 18. Caggiano V, Pomper JK, Fleischer F, Fogassi L, Giese M et al. Mirror neurons in monkey area F5 do not adapt to the observation of repeated actions. Nature Communications 2013; 4: 1433. https://doi.org/10.1038/ncomms2419
  • 19. Kilner JM, Kraskov A, Lemon RN. Do monkey F5 mirror neurons show changes in firing rate during repeated observation of natural actions? Journal of Neurophysiology 2014; 111: 1214- 1226. https://doi.org/10.1152/jn.01102.2012
  • 20. Hamilton AF, Grafton ST. Goal representation in human anterior intraparietal sulcus. Journal of Neuroscience 2006; 26: 1133-1137. https://doi.org/10.1523/jneurosci.4551-05.2006
  • 21. Cengiz B, Vurallı D, Zinnuroğlu M, Bayer G, Golmohammadzadeh H et al. Analysis of mirror neuron system activation during action observation alone and action observation with motor imagery tasks. Experimental Brain Research 2018; 236 (2): 497-503. https://doi.org/10.1007/ s00221-017-5147-5
  • 22. Faul F, Erdfelder E, Lang AG, Axel B. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods 2007; 39: 175-191. https://doi.org/10.3758/bf03193146
  • 23. Cavallo A, Becchio C, Sartori L, Bucchioni G, Castiello U. Grasping with tools: corticospinal excitability reflects observed hand movements. Cerebral Cortex 2012; 22 (3): 710-716. https://doi.org/10.1093/cercor/bhr157
  • 24. Fadiga L, Fogassi L, Pavesi G, Rizzolatti G. Motor facilitation during action observation: a magnetic stimulation study. Journal of Neurophysiology 1995; 73: 2608-2611. https://doi. org/10.1152/jn.1995.73.6.2608
  • 25. Gangitano M, Mottaghy F, Pascual-Leone A. Phase-specific modulation of cortical motor output during movement observation. NeuroReport 2001; 12: 1489-1492. https://doi. org/10.1097/00001756-200105250-00038
  • 26. Ito T, Tsubahara A, Shiraga Y, Yosuke Y, Daisuke K et al. Motor activation is modulated by visual experience during cyclic gait observation: a transcranial magnetic stimulation study. PLoS One 2020; 15 (1): e0228389. https://doi.org/10.1371/journal. pone.0228389
  • 27. Prinsen J, Alaerts K. Enhanced mirroring upon mutual gaze: multimodal evidence from TMS-assessed corticospinal excitability and the EEG mu rhythm. Scientific Reports 2020; 10 (1): 20449. https://doi.org/10.1038/s41598-020-77508-x
  • 28. Rens G, van Polanen V, Botta A, Gann MA, Orban de Xivry JJ et al. Sensorimotor expectations bias motor resonance during observation of object lifting: the causal role of pSTS. Journal of Neuroscience 2020; 40 (20): 3995-4009. https://doi.org/10.1523/ jneurosci.2672-19.2020
  • 29. Baldissera F, Cavallari P, Craighero L, Fadiga L. Modulation of spinal excitability during observation of hand actions in humans. European Journal of Neuroscience 2001; 13: 190-194. https://doi. org/10.1046/j.0953-816x.2000.01368.x
  • 30. Hari R, Forss N, Avikainen S, Veskari E, Salenius S et al. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proceedings of the National Academy of Sciences of the United States of America 1998; 95: 15061-15065. https://doi.org/10.1073/pnas.95.25.15061
  • 31. Strafella AP, Paus T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. NeuroReport 2000; 11: 2289-2292. https://doi. org/10.1097/00001756-200007140-00044
  • 32. Syrov N, Bredikhin D, Yakovlev L, Miroshnikov A, Kaplan A. Mu-desynchronization, N400 and corticospinal excitability during observation of natural and anatomically unnatural finger movements. Frontiers in Human Neuroscience 2022; 16: 973229. https://doi.org/10.3389/fnhum.2022.973229
  • 33. Hommel B, Musseler J, Aschersleben G, Prinz W. The theory of event coding (TEC): a framework for perception and action planning. Behavioral and Brain Sciences 2001; 24: 849-878. https:// doi.org/10.1017/s0140525x01000103
  • 34. Fogassi L, Ferrari PF, Gesierich B, Rozzi S, Chersi F et al. Parietal lobe: from action organization to intention understanding. Science 2005; 308: 662-667. https://doi.org/10.1126/science.1106138
  • 35. Naider-Steinhart S, Katz-Leurer M. Analysis of proximal and distal muscle activity during handwriting tasks. American Journal of Occupational Therapy 2007; 61 (4): 392-398. https://doi. org/10.5014/ajot.61.4.392
  • 36. Kuravi P, Caggiano V, Giese M, Vogels R. Repetition suppression for visual actions in the macaque superior temporal sulcus. Journal of Neurophysiology 2016; 115 (3): 1324-1337. https://doi. org/10.1152/jn.00849.2015
  • 37. Won SH, Kim JC, Oh DW. Effects of a novel walking training program with postural correction and visual feed-back on walking function in patients with post-stroke hemiparesis. Journal of Physical Therapy Science, 2015; 27: 2581-2583. https://doi. org/10.1589/jpts.27.2581
  • 38. Ezendam D, Bongers R, Jannink MJA. Systematic review of the effectiveness of mirror therapy in upper extremity function. Disability and Rehabilitation 2009; 31: 2135-2149. https://doi. org/10.3109/09638280902887768
  • 39. Arya KN, Pandian S, Kumar D, Puri V. Task-based mirror therapy augmenting motor recovery in poststroke hemiparesis: a randomized controlled trial. Journal of Stroke and Cerebrovascular Diseases 2015; 24: 1738-1748. https://doi. org/10.1016/j.jstrokecerebrovasdis.2015.03.026
  • 40. Dohle C, Pullen J, Nakaten A, Kust J, Rietz C et al. Mirror therapy promotes recovery from severe hemiparesis: a randomized controlled trial. Neurorehabilitation and Neural Repair 2009; 23: 209-217. https://doi.org/10.1177/1545968308324786
  • 41. Michielsen ME, Selles RW, van der Geest JN, Eckhardt M, Yavuzer G et al. Motor recovery and cortical reorganization after mirror therapy in chronic stroke patients: a phase II randomized controlled trial. Neurorehabilitation and Neural Repair 2011; 25: 223-233. https://doi.org/10.1177/1545968310385127
  • 42. Deconinck FJA, Smorenburg ARP, Benham A, Ledebt A, Feltham MG et al. Reflections on mirror therapy: a systematic review of the effect of mirror visual feedback on the brain. Neurorehabilitation and Neural Repair 2015; 29: 349-361. https://doi.org/10.1177/1545968314546134
  • 43. Külünkoğlu B, Erbahçeci F, Alkan A. A comparison of the effects of mirror therapy and phantom exercises on phantom limb pain. Turkish Journal of Medical Sciences 2019; 49 (1): 101-109. https://doi.org/10.3906/sag-1712-166
APA Boran H, Kılınç H, Cengiz B (2023). Mirror neuron activity depending on the content and stage of the observed action: a TMS study. , 1428 - 1437. 10.55730/1300-0144.5710
Chicago Boran H. Evren,Kılınç Hasan,Cengiz Bülent Mirror neuron activity depending on the content and stage of the observed action: a TMS study. (2023): 1428 - 1437. 10.55730/1300-0144.5710
MLA Boran H. Evren,Kılınç Hasan,Cengiz Bülent Mirror neuron activity depending on the content and stage of the observed action: a TMS study. , 2023, ss.1428 - 1437. 10.55730/1300-0144.5710
AMA Boran H,Kılınç H,Cengiz B Mirror neuron activity depending on the content and stage of the observed action: a TMS study. . 2023; 1428 - 1437. 10.55730/1300-0144.5710
Vancouver Boran H,Kılınç H,Cengiz B Mirror neuron activity depending on the content and stage of the observed action: a TMS study. . 2023; 1428 - 1437. 10.55730/1300-0144.5710
IEEE Boran H,Kılınç H,Cengiz B "Mirror neuron activity depending on the content and stage of the observed action: a TMS study." , ss.1428 - 1437, 2023. 10.55730/1300-0144.5710
ISNAD Boran, H. Evren vd. "Mirror neuron activity depending on the content and stage of the observed action: a TMS study". (2023), 1428-1437. https://doi.org/10.55730/1300-0144.5710
APA Boran H, Kılınç H, Cengiz B (2023). Mirror neuron activity depending on the content and stage of the observed action: a TMS study. Turkish Journal of Medical Sciences, 53(5), 1428 - 1437. 10.55730/1300-0144.5710
Chicago Boran H. Evren,Kılınç Hasan,Cengiz Bülent Mirror neuron activity depending on the content and stage of the observed action: a TMS study. Turkish Journal of Medical Sciences 53, no.5 (2023): 1428 - 1437. 10.55730/1300-0144.5710
MLA Boran H. Evren,Kılınç Hasan,Cengiz Bülent Mirror neuron activity depending on the content and stage of the observed action: a TMS study. Turkish Journal of Medical Sciences, vol.53, no.5, 2023, ss.1428 - 1437. 10.55730/1300-0144.5710
AMA Boran H,Kılınç H,Cengiz B Mirror neuron activity depending on the content and stage of the observed action: a TMS study. Turkish Journal of Medical Sciences. 2023; 53(5): 1428 - 1437. 10.55730/1300-0144.5710
Vancouver Boran H,Kılınç H,Cengiz B Mirror neuron activity depending on the content and stage of the observed action: a TMS study. Turkish Journal of Medical Sciences. 2023; 53(5): 1428 - 1437. 10.55730/1300-0144.5710
IEEE Boran H,Kılınç H,Cengiz B "Mirror neuron activity depending on the content and stage of the observed action: a TMS study." Turkish Journal of Medical Sciences, 53, ss.1428 - 1437, 2023. 10.55730/1300-0144.5710
ISNAD Boran, H. Evren vd. "Mirror neuron activity depending on the content and stage of the observed action: a TMS study". Turkish Journal of Medical Sciences 53/5 (2023), 1428-1437. https://doi.org/10.55730/1300-0144.5710