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ORIGINAL RESEARCH ARTICLE

Functional features of the mirror neuron system during action observation and execution in patients with anxiety and depressive symptoms

Ekaterina D. Karimova1,2* ,  Sabir E. Burkitbayev1,2 ,  Mikhail S. Zinchuk2 ,  Alla B. Guekht2,3
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1 Laboratory of Applied Physiology of Human Higher Nervous Activity, Institute of Higher Nervous Activity and Neurophysiology (IHNA & NPh)n Academy of Sciences (RAS), Moscow, Russia
2 Scientific and Practical Center for Psychoneurology of the Moscow City Health Department, Moscow, Russia
3 Department of Neurology, Neurosurgery and Medical Genetics, Faculty of Medicine, Pirogov Russian National Research Medical University, Moscow, Russia
Advanced Neurology 2024, 3(1), 2009 https://doi.org/10.36922/an.2009
Submitted: 11 October 2023 | Accepted: 3 January 2024 | Published: 19 March 2024
© 2024 by the Author (s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

The perception and comprehension of non-verbal information and body language in humans and higher primates are realized by the mirror neuron system (MNS). Anxiety and depressive symptoms may change social perception, which could manifest as functional changes in the MNS. In this paper, using the inverse electroencephalography (EEG) problem and rhythm suppression, we investigated spatial and frequency distortions of the MNS in 24 patients exhibiting depressive and anxiety symptoms and 23 controls. EEG was recorded during four motor tasks: action observation (where participants observed a hand gesture performed by a demonstrator), imagination, execution, and joint execution (simultaneous execution with the demonstrator). Mu suppression was employed across a wide frequency and spatial range to assess the level of MNS activity, while the sLORETA method was employed to localize the activity sources. The results indicate that the patients demonstrated task-selective mu suppression mainly during observation and joint execution in the frontal, central, and occipital areas of the cortex across a wide frequency range. In contrast, the controls demonstrated clear and pronounced mu rhythm suppression in the central regions of the brain in the upper-frequency range (10.5 – 13 Hz) during all mirroring tasks. These results suggest that patients with anxiety and depressive symptoms engage additional neural resources to complete social tasks, particularly involving auxiliary neural networks located in the frontal associative arrays and visual cortex.

Keywords
Anxiety
Depression
Mirror neurons
Electroencephalography
Social perception
Communication
Funding
This article was fully prepared in accordance with the state assignment of the Ministry of Education and Science of the Russian Federation for 2019 – 2021 (No. 1201371233).
Conflict of interest
The authors declare no conflicts of interests.
References
  1. Vahratian A, Blumberg SJ, Terlizzi EP, Schiller JS. Symptoms of anxiety or depressive disorder and use of mental health care among adults during the COVID-19 pandemic-united states, August 2020-February 2021. MMWR Morb Mortal Wkly Rep. 2021;70(13):490-494. doi: 10.15585/mmwr.mm7013e2

 

  1. Coretti S, Rumi F, Cicchetti A. The social cost of major depression. A systematic review. Rev Eur Stud. 2019;11(1):73-85. doi: 10.5539/res.v11n1p73

 

  1. Kupferberg A, Bicks L, Hasler G. Social functioning in major depressive disorder. Neurosci Biobehav Rev. 2016;69: 313-332. doi: 10.1016/j.neubiorev.2016.07.002

 

  1. Bonini L, Rotunno C, Arcuri E, Gallese V. Mirror neurons 30 years later: Implications and applications. Trends Cogn Sci. 2022;26(9):767-781. doi: 10.1016/j.tics.2022.06.003

 

  1. Rizzolatti G, Fadiga L, Gallese V, Fogassi L. Premotor cortex and the recognition of motor actions. Brain Res Cogn Brain Res. 1996;3(2):131-141. doi: 10.1016/0926-6410(95)00038-0

 

  1. Mikulan EP, Reynaldo L, Ibáñez A. Homuncular mirrors: Misunderstanding causality in embodied cognition. Front Hum Neurosci. 2014;8:299. doi: 10.3389/fnhum.2014.00299

 

  1. Rizzolatti G, Craighero L. The mirror-neuron system. Annu Rev Neurosci. 2004;27(1):169-192. doi: 10.1146/annurev.neuro.27.070203.144230

 

  1. Hutchison WD, Davis KD, Lozano AM, Tasker RR, Dostrovsky JO. Pain-related neurons in the human cingulate cortex. Nat Neurosci. 1999;2(5):403-405. doi: 10.1038/8065

 

  1. Singer T, Seymour B, O’Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science. 2004; 303(5661):1157-1162. doi: 10.1126/science.1093535

 

  1. Carr L, Iacoboni M, Dubeau MC, Mazziotta JC, Lenzi GL. Neural mechanisms of empathy in humans: A relay from neural systems for imitation to limbic areas. Proc Natl Acad Sci U S A. 2003;100(9):5497-5502. doi: 10.1073/pnas.0935845100

 

  1. Calvo-Merino B, Glaser DE, Grèzes J, Passingham RE, Haggard P. Action observation and acquired motor skills: An fMRI study with expert dancers. Cereb Cortex. 2005;15(8):1243-1249. doi: 10.1093/cercor/bhi007

 

  1. Grèzes J, Decety J. Functional anatomy of execution, mental simulation, observation, and verb generation of actions: A meta-analysis. Hum Brain Mapp. 2001;12(1):1-19. doi: 10.1002/1097-0193(200101)12:1<1:aid-hbm10>3.0.co;2-v

 

  1. Rizzolatti G, Sinigaglia C. The mirror mechanism: A basic principle of brain function. Nat Rev Neurosci. 2016;17(12):757-765. doi: 10.1038/nrn.2016.135

 

  1. Debnath R, Salo VC, Buzzell GA, Yoo KH, Fox NA. Mu rhythm desynchronization is specific to action execution and observation: Evidence from time-frequency and connectivity analysis. Neuroimage. 2019;184:496-507. doi: 10.1016/j.neuroimage.2018.09.053

 

  1. Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I. Single-neuron responses in humans during execution and observation of actions. Curr Biol. 2010;20(8):750-756. doi: 10.1016/j.cub.2010.02.045

 

  1. Fox NA, Yoo KH, Bowman LC, et al. Assessing human mirror activity With EEG mu rhythm: A meta-analysis. Psychol Bull. 2016;142(3):291-313. doi: 10.1037/bul0000031

 

  1. Larionova EV, Garakh ZV, Zaytseva YS. The mu rhythm in current research: Theoretical and methodological aspects. Neurosci Behav Physiol. 2022;52(7):999-1016. doi: 10.1007/s11055-022-01329-w

 

  1. Yin S, Liu Y, Ding M. Amplitude of sensorimotor mu rhythm is correlated with BOLD from multiple brain regions: A simultaneous EEG-fMRI study. Front Hum Neurosci. 2016;10:364. doi: 10.3389/fncel.2016.00364

 

  1. Frenkel-Toledo S, Bentin S, Perry A, Liebermann DG, Soroker N. Mirror-neuron system recruitment by action observation: Effects of focal brain damage on mu suppression. Neuroimage. 2014;87:127-137. doi: 10.1016/j.neuroimage.2013.10.019

 

  1. Bimbi M, Festante F, Coudé G, Vanderwert RE, Fox NA, Ferrari PF. 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. 2018;175:22-31. doi: 10.1016/j.neuroimage.2018.03.037

 

  1. Charidza CA, Gillmeister H. Differential beta desynchronisation responses to dynamic emotional facial expressions are attenuated in higher trait anxiety and autism. Cogn Affect Behav Neurosci. 2022;22(6):1404-1420. doi: 10.3758/s13415-022-01015-x

 

  1. Hobson HM, Bishop DVM. Mu suppression-A good measure of the human mirror neuron system? Cortex. 2016;82:290-310. doi: 10.1016/j.cortex.2016.03.019

 

  1. Hobson HM, Bishop DVM. The interpretation of mu suppression as an index of mirror neuron activity: Past, present and future. R Soc Open Sci. 2017;4(3):160662. doi: 10.1098/rsos.160662

 

  1. Chuang J, Nguyen H, Wang C, Johnson B. I think, therefore I am: Usability and security of authentication using brainwaves. In: Lecture Notes in Computer Science (Including Subseries Lecture Notes in Artificial Intelligence and Lecture Notes in Bioinformatics). Berlin, Heidelberg: Springer;2013. doi: 10.1007/978-3-642-41320-9_1

 

  1. Saffin JM, Tohid H. Walk like me, talk like me. The connection between mirror neurons and autism spectrum disorder. Neuroscience (Riyadh). 2016;21(2):108-119. doi: 10.17712/nsj.2016.2.20150472

 

  1. Chan MMY, Han YMY. Differential mirror neuron system (MNS) activation during action observation with and without social-emotional components in autism: A meta-analysis of neuroimaging studies. Mol Autism. 2020; 11(1):72. doi: 10.1186/s13229-020-00374-x

 

  1. Zhao W, Liu Q, Zhang X, et al. Differential responses in the mirror neuron system during imitation of individual emotional facial expressions and association with autistic traits. Neuroimage. 2023;277:120263. doi: 10.1016/j.neuroimage.2023.120263

 

  1. Horan WP, Pineda JA, Wynn JK, Iacoboni M, Green MF. Some markers of mirroring appear intact in schizophrenia: Evidence from mu suppression. Cogn Affect Behav Neurosci. 2014;14(3):1049-1060. doi: 10.3758/s13415-013-0245-8

 

  1. Lee JS, Chun JW, Yoon SY, Park HJ, Kim JJ. Involvement of the mirror neuron system in blunted affect in schizophrenia. Schizophr Res. 2014;152(1):268-274. doi: 10.1016/j.schres.2013.10.043

 

  1. Bagewadi VI, Mehta UM, Naik SS, et al. Diminished modulation of motor cortical reactivity during context-based action observation in schizophrenia. Schizophr Res. 2019;204:222-229. doi: 10.1016/j.schres.2018.07.043

 

  1. Valizadeh A, Mbwogge M, Yazdi AR, et al. The mirror mechanism in schizophrenia: A systematic review and qualitative meta-analysis. Front Psychiatry. 2022;13:884828. doi: 10.3389/fpsyt.2022.884828.

 

  1. Mier D, Lis S, Esslinger C, et al. Neuronal correlates of social cognition in borderline personality disorder. Soc Cogn Affect Neurosci. 2013;8(5):531-537. doi: 10.1093/scan/nss028

 

  1. Sosic-Vasic Z, Eberhardt J, Bosch JE, et al. Mirror neuron activations in encoding of psychic pain in borderline personality disorder. Neuroimage Clin. 2019;22:101737. doi: 10.1016/j.nicl.2019.101737

 

  1. Andrews SC, Enticott PG, Hoy KE, Thomson RH, Fitzgerald PB. Reduced mu suppression and altered motor resonance in euthymic bipolar disorder: Evidence for a dysfunctional mirror system? Soc Neurosci. 2016;11(1):60-71. doi: 10.1080/17470919.2015.1029140

 

  1. Kim E, Jung YC, Ku J, et al. Reduced activation in the mirror neuron system during a virtual social cognition task in euthymic bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2009;33(8):1409-1416. doi: 10.1016/j.pnpbp.2009.07.019

 

  1. Bodnar A, Rybakowski JK. Increased affective empathy in bipolar patients during a manic episode. Braz J Psychiatry. 2017;39(4):342-345. doi: 10.1590/1516-4446-2016-2101

 

  1. Mehta UM, Thirthalli J, Aneelraj D, Jadhav P, Gangadhar BN, Keshavan MS. Mirror neuron dysfunction in schizophrenia and its functional implications: A systematic review. Schizophr Res. 2014;160(1-3):9-19. doi: 10.1016/j.schres.2014.10.040

 

  1. Basavaraju R, Mehta UM, Thirthalli J. Elevated mirror neuron system activity is associated with impaired theory of mind in mania. Asian J Psychiatr. 2020;47:101862. doi: 10.1016/j.ajp.2019.101862

 

  1. Basavaraju R, Mehta UM, Pascual‐Leone A, Thirthalli J. Elevated mirror neuron system activity in bipolar mania: Evidence from a transcranial magnetic stimulation study. Bipolar Disord. 2019;21(3):259-269. doi: 10.1111/bdi.12723

 

  1. Kumar P, Waiter GD, Dubois M, Milders M, Reid I, Steele JD. Increased neural response to social rejection in major depression. Depress Anxiety. 2017;34(11):1049-1056. doi: 10.1002/da.22665

 

  1. Suffel A, Nagels A, Steines M, Kircher T, Straube B. Feeling addressed! The neural processing of social communicative cues in patients with major depression. Hum Brain Mapp. 2020;41(13):3541-3554. doi: 10.1002/hbm.25027

 

  1. Jahangard L, Tayebi M, Haghighi M, et al. Does rTMS on brain areas of mirror neurons lead to higher improvements on symptom severity and empathy compared to the rTMS standard procedure?-Results from a double-blind interventional study in individuals with major depressive disorders. J Affect Disord. 2019;257:527-535. doi: 10.1016/j.jad.2019.07.019

 

  1. Washburn D, Wilson G, Roes M, Rnic K, Harkness KL. Theory of mind in social anxiety disorder, depression, and comorbid conditions. J Anxiety Disord. 2016;37:71-77. doi: 10.1016/j.janxdis.2015.11.004

 

  1. Buccino G, Amore M. Mirror neurons and the understanding of behavioural symptoms in psychiatric disorders. Curr Opin Psychiatry. 2008;21(3):281-285. doi: 10.1097/YCO.0b013e3282fbcd32

 

  1. Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J. An inventory for measuring depression. Arch Gen Psychiatry. 1961;4(6):561-571. doi: 10.1001/archpsyc.1961.01710120031004

 

  1. Skapinakis P. Spielberger state-trait anxiety inventory. In: Encyclopedia of Quality of Life and Well-Being Research. Netherlands: Springer; 2014. p. 6261-6264. doi: 10.1007/978-94-007-0753-5_2825

 

  1. Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS. A standardized boundary element method volume conductor model. Clin Neurophysiol. 2002;113(5):702-712. doi: 10.1016/S1388-2457(02)00030-5

 

  1. Jurcak V, Tsuzuki D, Dan I. 10/20, 10/10, and 10/5 systems revisited: Their validity as relative head-surface-based positioning systems. Neuroimage. 2007;34(4):1600-1611. doi: 10.1016/j.neuroimage.2006.09.024

 

  1. Pascual-Marqui RD. Standardized low-resolution brain electromagnetic tomography (sLORETA): Technical details. Methods Find Exp Clin Pharmacol. 2002;24(Suppl D): 5-12.

 

  1. Karimova E, Burkitbaev S, Katermin N. The Mirror Neuron System Activity is Higher with Personal Direct Interaction. Berlin: Springer Nature; 2021. p. 114-121. doi: 10.1007/978-3-030-71637-0_13

 

  1. Lebedeva NN, Karimova ED, Kazimirova EA, Vehov AV. Complex neurophysiological examination of patients with affective disorders. Zh Vyssh Nerv Deiat Im I P Pavlova. 2015;65(3):313-323.

 

  1. Haghighi M, Ludyga S, Rahimi B, et al. In patients suffering from major depressive disorders, quantitative EEG showed favorable changes in left and right prefrontal cortex. Psychiatry Res. 2017;251:137-141. doi: 10.1016/j.psychres.2017.02.012

 

  1. Hughes JR. A review of the usefulness of the standard EEG in psychiatry. Clin Electroencephalogr. 1996;27(1):35-39. doi: 10.1177/155005949602700106

 

  1. Korb AS, Cook IA, Hunter AM, Leuchter AF. Brain electrical source differences between depressed subjects and healthy controls. Brain Topogr. 2008;21(2):138-146. doi: 10.1007/s10548-008-0070-5

 

  1. Northoff G. How do resting state changes in depression translate into psychopathological symptoms? From ‘spatiotemporal correspondence’ to ‘spatiotemporal psychopathology’. Curr Opin Psychiatry. 2016;29(1):18-24. doi: 10.1097/YCO.0000000000000222

 

  1. Pizzagalli DA, Oakes TR, Davidson RJ. Coupling of theta activity and glucose metabolism in the human rostral anterior cingulate cortex: An EEG/PET study of normal and depressed subjects. Psychophysiology. 2003;40(6):939-949. doi: 10.1111/1469-8986.00112

 

  1. Shim M, Im CH, Kim YW, Lee SH. Altered cortical functional network in major depressive disorder: A resting-state electroencephalogram study. Neuroimage Clin. 2018;19:1000-1007. doi: 10.1016/j.nicl.2018.06.012

 

  1. Kemmerer D. What modulates the mirror neuron system during action observation?: Multiple factors involving the action, the actor, the observer, the relationship between actor and observer, and the context. Prog Neurobiol. 2021;205:102128. doi: 10.1016/j.pneurobio.2021.102128

 

  1. Ferrari PF, Gerbella M, Coudé G, Rozzi S. Two different mirror neuron networks: The sensorimotor (hand) and limbic (face) pathways. Neuroscience. 2017;358:300-315. doi: 10.1016/j.neuroscience.2017.06.052

 

  1. Chen W, Yuan T, Wang Y, Ding J. Human mirror neuron system and its plasticity. Neural Regen Res. 2008;3(3):321-323.

 

  1. Catmur C, Walsh V, Heyes C. Sensorimotor learning configures the human mirror system. Curr Biol. 2007;17(17): 1527-1531. doi: 10.1016/j.cub.2007.08.006

 

  1. Buccino G, Solodkin A, Small SL. Functions of the mirror neuron system: Implications for neurorehabilitation. Cogn Behav Neurol. 2006;19(1):55-63. doi: 10.1097/00146965-200603000-00007

 

  1. Mehta UM, Waghmare AV, Thirthalli J, Venkatasubramanian G, Gangadhar BN. Is the human mirror neuron system plastic? Evidence from a transcranial magnetic stimulation study. Asian J Psychiatr. 2015;17:71-77. doi: 10.1016/j.ajp.2015.06.014

 

  1. Bagewadi VI, Mehta UM, Sundar AS, Kumar CN, Thirthalli J. Exploring modulation of mirror neuron activity with a novel emotionally embedded motor task and its associations with social cognition in schizophrenia. Brain Stimul. 2015;8(2):354. doi: 10.1016/j.brs.2015.01.144

 

  1. Tramacere A, Pievani T, Ferrari PF. Mirror neurons in the tree of life: Mosaic evolution, plasticity and exaptation of sensorimotor matching responses. Biol Rev Camb Philos Soc. 2017;92(3):1819-1841. doi: 10.1111/brv.12310

 

  1. Karimova ED, Gulyaeva AS, Katermin NS. The degree of mu rhythm suppression in women is associated with presence of children as well as empathy and anxiety level. Soc Neurosci. 2022;17(4):382-396. doi: 10.1080/17470919.2022.2112753

 

  1. Lebedeva N, Gulyaeva N, Akzhigitov R, et al. Neurophysiologic correlates of depression and anxiety. J Neurol Sci. 2015;357(1):e240-e241. doi: 10.1016/j.jns.2015.08.841

 

  1. Balderston NL, Vytal KE, O’Connell K, et al. Anxiety patients show reduced working memory related dlPFC activation during safety and threat. Depress Anxiety. 2017;34(1):25-36. doi: 10.1002/da.22518

 

  1. Keller AS, Leikauf JE, Holt-Gosselin B, Staveland BR, Williams LM. Paying attention to attention in depression. Transl Psychiatry. 2019;9(1):279. doi: 10.1038/s41398-019-0616-1

 

  1. Schweizer S, Kievit RA, Emery T, Cam-CAN, Henson RN. Symptoms of depression in a large healthy population cohort are related to subjective memory complaints and memory performance in negative contexts. Psychol Med. 2018;48(1):104-114. doi: 10.1017/S0033291717001519

 

  1. Di Gregorio F, La Porta F, Petrone V, et al. Accuracy of EEG biomarkers in the detection of clinical outcome in disorders of consciousness after severe acquired brain injury: Preliminary results of a pilot study using a machine learning approach. Biomedicines. 2022;10(8):1897. doi: 10.3390/biomedicines10081897

 

  1. Turri C, Di Dona G, Santoni A, et al. Periodic and aperiodic EEG Features as potential markers of developmental dyslexia. Biomedicines. 2023;11(6):1607. doi: 10.3390/biomedicines11061607

 

  1. Mehta UM, Basavaraju R, Thirthalli J. Motor cortical reactivity to action observation: A biomarker to differentiate mania and schizophrenia? Schizophr Res. 2019;211:95-97. doi: 10.1016/j.schres.2019.07.044
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