Is there a relationship between EEG and sTMS neurophysiological markers of the putative human mirror neuron system?


Journal

Journal of neuroscience research
ISSN: 1097-4547
Titre abrégé: J Neurosci Res
Pays: United States
ID NLM: 7600111

Informations de publication

Date de publication:
12 2021
Historique:
revised: 31 08 2021
received: 13 12 2020
accepted: 03 09 2021
pubmed: 9 11 2021
medline: 1 4 2022
entrez: 8 11 2021
Statut: ppublish

Résumé

The mirror neuron system (MNS) has been theorized to play a neurobiological role in a number of social cognitive abilities and is commonly indexed putatively in humans via interpersonal motor resonance (IMR) and mu suppression. Although both indices are thought to measure similar neuronal populations (i.e., "mirror neurons"), it has been suggested that these methods are unrelated, and therefore, incompatible. However, prior studies reporting no relationships were typically conducted in small and underpowered samples. Thus, we aimed to investigate this potential association in a large sample of neurotypical adults (N = 116; 72 females). Participants underwent transcranial magnetic stimulation (TMS), electromyography (EMG), and electroencephalography (EEG) during the observation of videos of actors performing grasping actions in order to index IMR and mu suppression (in beta, lower alpha, and upper alpha bandwidths). A series of linear regressions revealed no associations between IMR and each of the mu suppression bandwidths. Supplementary Bayesian analyses provided further evidence in favor of the null (B

Identifiants

pubmed: 34747052
doi: 10.1002/jnr.24969
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

3238-3249

Informations de copyright

© 2021 Wiley Periodicals LLC.

Références

Arnstein, D., Cui, F., Keysers, C., Maurits, N. M., & Gazzola, V. (2011). μ-suppression during action observation and execution correlates with BOLD in dorsal premotor, inferior parietal, and SI cortices. Journal of Neuroscience, 31, 14243-14249. https://doi.org/10.1523/JNEUROSCI.0963-11.2011
Bekkali, S., Youssef, G. J., Donaldson, P. H., Albein-Urios, N., Hyde, C., & Enticott, P. G. (2020). Is the putative mirror neuron system associated with empathy? A systematic review and meta-analysis. Neuropsychology Review, 31(1), 14-57.
Bekkali, S., Youssef, G. J., Donaldson, P. H., He, J., Do, M., Hyde, C., Barhoun, P., & Enticott, P. G. (2020). Do gaze behaviours during action observation predict interpersonal motor resonance? Social Cognitive and Affective Neuroscience, nsaa106. https://doi.org/10.1093/scan/nsaa106
Bimbi, M., Festante, F., Coudé, G., Vanderwert, R. E., Fox, N. A., & Ferrari, P. F. (2018). Simultaneous scalp recorded EEG and local field potentials from monkey ventral premotor cortex during action observation and execution reveals the contribution of mirror and motor neurons to the mu rhythm. Neuroimage, 175, 22-31. https://doi.org/10.1016/j.neuroimage.2018.03.037
Buccino, G., & Amore, M. (2008). Mirror neurons and the understanding of behavioural symptoms in psychiatric disorders. Current Opinion in Psychiatry, 21(3), 281-285. https://doi.org/10.1097/YCO.0b013e3282fbcd32
Buccino, G., & Riggio, L. (2006). The role of the mirror neuron system in motor learning. Kinesiology, 38(1), 5-15.
Buccino, G., Solodkin, A., & Small, S. L. (2006). Functions of the mirror neuron system: Implications for neurorehabilitation. Cognitive and Behavioral Neurology, 19(1), 55-63. https://doi.org/10.1097/00146965-200603000-00007
Cole, E. J., Barraclough, N. E., & Enticott, P. G. (2018). Investigating mirror system (MS) activity in adults with ASD when inferring others’ intentions using both TMS and EEG. Journal of Autism and Developmental Disorders, 48(7), 2350-2367. https://doi.org/10.1007/s10803-018-3492-2
Enticott, P. G., Kennedy, H. A., Bradshaw, J. L., Rinehart, N. J., & Fitzgerald, P. B. (2010). Understanding mirror neurons: Evidence for enhanced corticospinal excitability during the observation of transitive but not intransitive hand gestures. Neuropsychologia, 48(9), 2675-2680. https://doi.org/10.1016/j.neuropsychologia.2010.05.014
Fadiga, L., Fogassi, L., Pavesi, G., & Rizzolatti, G. (1995). Motor facilitation during action observation: A magnetic stimulation study. Journal of Neurophysiology, 73(6), 2608-2611. https://doi.org/10.1152/jn.1995.73.6.2608
Faul, F., Erdfelder, E., Lang, A.-G., & Buchner, A. (2007). G* Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175-191. https://doi.org/10.3758/BF03193146
Faulkenberry, T. J. (2018). Computing Bayes factors to measure evidence from experiments: An extension of the BIC approximation. Biometrical Letters, 55(1), 31-43. https://doi.org/10.2478/bile-2018-0003
Fogassi, L., & Ferrari, P. F. (2007). Mirror neurons and the evolution of embodied language. Current Directions in Psychological Science, 16(3), 136-141. https://doi.org/10.1111/j.1467-8721.2007.00491.x
Fuelscher, I., Caeyenberghs, K., Enticott, P. G., Kirkovski, M., Farquharson, S., Lum, J., & Hyde, C. (2019). Does fMRI repetition suppression reveal mirror neuron activity in the human brain? Insights from univariate and multivariate analysis. European Journal of Neuroscience, 50, 2877-2892. https://doi.org/10.1111/ejn.14370
Gangitano, M., Mottaghy, F. M., & Pascual-Leone, A. (2001). Phase-specific modulation of cortical motor output during movement observation. NeuroReport, 12(7), 1489-1492. https://doi.org/10.1097/00001756-200105250-00038
Gonzalez-Liencres, C., Shamay-Tsoory, S. G., & Brüne, M. (2013). Towards a neuroscience of empathy: Ontogeny, phylogeny, brain mechanisms, context and psychopathology. Neuroscience & Biobehavioral Reviews, 37(8), 1537-1548. https://doi.org/10.1016/j.neubiorev.2013.05.001
Hobson, H. M., & Bishop, D. V. (2016). Mu suppression-A good measure of the human mirror neuron system? Cortex, 82, 290-310. https://doi.org/10.1016/j.cortex.2016.03.019
Hyde, C., Fuelscher, I., Williams, J., Lum, J. A., He, J., Barhoun, P., & Enticott, P. G. (2018). Corticospinal excitability during motor imagery is reduced in young adults with developmental coordination disorder. Research in Developmental Disabilities, 72, 214-224.
Iacoboni, M. (2009). Imitation, empathy, and mirror neurons. Annual Review of Psychology, 60, 653-670. https://doi.org/10.1146/annurev.psych.60.110707.163604
Jeon, H., & Lee, S.-H. (2018). From neurons to social beings: Short review of the mirror neuron system research and its socio-psychological and psychiatric implications. Clinical Psychopharmacology and Neuroscience, 16(1), 18-31. https://doi.org/10.9758/cpn.2018.16.1.18
Lamm, C., & Majdandzic, J. (2015). The role of shared neural activations, mirror neurons, and morality in empathy-A critical comment. Neuroscience Research, 90, 15-24. https://doi.org/10.1016/j.neures.2014.10.008
Lapenta, O. M., Ferrari, E., Boggio, P. S., Fadiga, L., & D’Ausilio, A. (2018). Motor system recruitment during action observation: No correlation between mu rhythm desynchronization and corticospinal excitability. PLoS ONE, 13(11), e0207476. https://doi.org/10.1371/journal.pone.0207476
Lepage, J.-F., Saint-Amour, D., & Théoret, H. (2008). EEG and neuronavigated single-pulse TMS in the study of the observation/execution matching system: Are both techniques measuring the same process? Journal of Neuroscience Methods, 175(1), 17-24. https://doi.org/10.1016/j.jneumeth.2008.07.021
Lepage, J.-F., Tremblay, S., & Théoret, H. (2010). Early non-specific modulation of corticospinal excitability during action observation. European Journal of Neuroscience, 31(5), 931-937. https://doi.org/10.1111/j.1460-9568.2010.07121.x
Li, C.-H. (2016). Confirmatory factor analysis with ordinal data: Comparing robust maximum likelihood and diagonally weighted least squares. Behavior Research Methods, 48(3), 936-949. https://doi.org/10.3758/s13428-015-0619-7
Mäki, H., & Ilmoniemi, R. J. (2010). EEG oscillations and magnetically evoked motor potentials reflect motor system excitability in overlapping neuronal populations. Clinical Neurophysiology, 121(4), 492-501. https://doi.org/10.1016/j.clinph.2009.11.078
Muthén, L., & Muthén, B. (2012). Mplus user’s guide (1998-2012) (Vol. 6). Author.
Muthukumaraswamy, S. D., Johnson, B. W., & McNair, N. A. (2004). Mu rhythm modulation during observation of an object-directed grasp. Cognitive Brain Research, 19(2), 195-201. https://doi.org/10.1016/j.cogbrainres.2003.12.001
Oberman, L. M., Hubbard, E. M., McCleery, J. P., Altschuler, E. L., Ramachandran, V. S., & Pineda, J. A. (2005). EEG evidence for mirror neuron dysfunction in autism spectrum disorders. Cognitive Brain Research, 24(2), 190-198. , http://ezproxy.deakin.edu.au/login?url=http://search.ebscohost.com/login.aspx?direct=true&db=mdc&AN=15993757&site=ehost-live&scope=site http://ac.els-cdn.com/S0926641005000224/1-s2.0-S0926641005000224-main.pdf?_tid=10ebb336-861a-11e6-9fca-00000aacb362&acdnat=1475135899_44ff9eac509fa8139ae0b29027c94460 https://doi.org/10.1016/j.cogbrainres.2005.01.014
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia, 9(1), 97-113. https://doi.org/10.1016/0028-3932(71)90067-4
Pascual-Leone, A. (1999). Transcranial magnetic stimulation: Studying the brain-behaviour relationship by induction of ‘virtual lesions’. Philosophical Transactions of the Royal Society B: Biological Sciences, 354(1387), 1229-1238.
Prinsen, J., & Alaerts, K. (2020). Enhanced mirroring upon mutual gaze: Multimodal evidence from TMS-assessed corticospinal excitability and the EEG mu rhythm. bioRxiv.
Raftery, A. E. (1995). Bayesian model selection in social research. Sociological Methodology, 25, 111-163. https://doi.org/10.2307/271063
Rizzolatti, G., & Craighero, L. (2004). The mirror-neuron system. Annual Review of Neuroscience, 27, 169-192. https://doi.org/10.1146/annurev.neuro.27.070203.144230
Rossi, S., Hallett, M., Rossini, P. M., & Pascual-Leone, A., & Safety of TMS Consensus Group. (2009). Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clinical Neurophysiology, 120(12), 2008-2039. https://doi.org/10.1016/j.clinph.2009.08.016
Sakreida, K., Effnert, I., Thill, S., Menz, M. M., Jirak, D., Eickhoff, C. R., Ziemke, T., Eickhoff, S. B., Borghi, A. M., & Binkofski, F. (2016). Affordance processing in segregated parieto-frontal dorsal stream sub-pathways. Neuroscience & Biobehavioral Reviews, 69, 89-112. https://doi.org/10.1016/j.neubiorev.2016.07.032
Schafer, J. L., & Graham, J. W. (2002). Missing data: Our view of the state of the art. Psychological Methods, 7(2), 147-177. https://doi.org/10.1037/1082-989X.7.2.147
Schmidt, S., Cichy, R., Kraft, A., Brocke, J., Irlbacher, K., & Brandt, S. (2009). An initial transient-state and reliable measures of corticospinal excitability in TMS studies. Clinical Neurophysiology, 120(5), 987-993. https://doi.org/10.1016/j.clinph.2009.02.164
Strafella, A. P., & Paus, T. (2000). Modulation of cortical excitability during action observation: A transcranial magnetic stimulation study. NeuroReport, 11(10), 2289-2292. https://doi.org/10.1097/00001756-200007140-00044
Uithol, S., van Rooij, I., Bekkering, H., & Haselager, P. (2011). Understanding motor resonance. Social Neuroscience, 6(4), 388-397. https://doi.org/10.1080/17470919.2011.559129
Van de Schoot, R., Yerkes, M. A., Mouw, J. M., & Sonneveld, H. (2013). What took them so long? Explaining PhD delays among doctoral candidates. PLoS ONE, 8(7), e68839. https://doi.org/10.1371/journal.pone.0068839
Wagenmakers, E.-J. (2007). A practical solution to the pervasive problems ofp values. Psychonomic Bulletin & Review, 14(5), 779-804. https://doi.org/10.3758/BF03194105
Zhu, H., Sun, Y., & Wang, F. (2013). Electroencephalogram evidence for the activation of human mirror neuron system during the observation of intransitive shadow and line drawing actions. Neural Regeneration Research, 8(3), 251.

Auteurs

Soukayna Bekkali (S)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

George J Youssef (GJ)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.
Centre for Adolescent Health, Murdoch Children's Research Institute, Parkville, Melbourne, VIC, Australia.

Peter H Donaldson (PH)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

Christian Hyde (C)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

Michael Do (M)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

Jason L He (JL)

Department of Forensic and Neurodevelopmental Sciences, Sackler Institute for Translational Neurodevelopment, Institute of Psychiatry, Psychology, and Neuroscience, King's College London, London, UK.

Pamela Barhoun (P)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

Peter G Enticott (PG)

Cognitive Neuroscience Unit (CNU), School of Psychology, Deakin University, Burwood, VIC, Australia.

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