Localization of Sources Generating the EEG α Rhythm during Observation, Performance, and Imitation of Operant Movements in Subjects with Different Intelligence Levels

Use of the sLORETA method in 62 adult subjects with different intelligence levels located sources generating rhythms in the frequency band 8–12 Hz during observation, performance, and imitation of circular movements with a computer mouse by the experimenter. A relationship between the level of intelligence and differences in the spatial patterns of cerebral cortex activation during performance and imitation of movements was seen. More marked and localized activation of neocortical structures was seen in adult subjects with high levels of general intelligence. Differences in the activation of cortical areas in groups with different general intelligence levels were largely mediated by structures in the right hemisphere, which is involved in processes of visuomotor coordination and the discrimination of own from others’ actions. The greater involvement of the precentral, cingulate, and postcentral gyri of the left hemisphere in the process of imitating the experimenter’s movements in the group with high intelligence may point to a higher level of activation of the mirror system of the brain.

This is a preview of subscription content, access via your institution.

References

  1. Alikina, M. A., Makhin, S. A., and Pavlenko, V. B., “People with high levels of general intelligence demonstrate more marked desynchronization of the μ rhythm on observation of the actions of others,” Uch. Zapis. Krym. Fed. Univ. im. Vernadskogo. Biol. Khim., 4, No. 3, 26–34 (2018).

    Google Scholar 

  2. Anwar, M. N., Navid, S. N., Khan, M., and Kitajo, K., “A possible correlation between performance IQ, visuomotor adaptation ability and mu suppression,” Brain Res., 1603, No. 7, 84–93 (2015).

    CAS  PubMed  Google Scholar 

  3. Banker, L. and Tadi, P., Neuroanatomy. Precentral Gyrus, StatPearls Publishing (2019).

  4. Brass, M., Ruby, P., and Spengler, S., “Inhibition of imitative behaviour and social cognition,” Philos. Trans. R. Soc. Lond. B Biol. Sci., 364, No. 1528, 2359–2367 (2009).

    PubMed  PubMed Central  Google Scholar 

  5. Campbell, M. E. J., Mehrkanoon, S., and Cunnington, R., “Intentionally not imitating: Insula cortex engaged for top-down control of action mirroring,” Neuropsychologia, 111, 241–251 (2018).

    PubMed  Google Scholar 

  6. Candidi, M., Urgesi, C., Ionta, S., and Aglioti, S. M., “Virtual lesion of ventral premotor cortex impairs visual perception of biomechanically possible but not impossible actions,” Soc. Neurosci., 3, No. 3–4, 388–400 (2008).

    PubMed  Google Scholar 

  7. Cavanna, A. and Trimble, M., “The precuneus: a review of its functional anatomy and behavioural correlates,” Brain, 129, No. 3, 564–583 (2006).

    PubMed  Google Scholar 

  8. Cross, K. A., Torrisi, S., Reynolds Losin, E. A., and Iacoboni, M., “Controlling automatic imitative tendencies: Interactions between mirror neuron and cognitive control systems,” NeuroImage, 83, 493–504 (2013).

    PubMed  PubMed Central  Google Scholar 

  9. de Munck, J. C., Gonçalves, S. I., Mammoliti, R., et al., “Interactions between different EEG frequency bands and their effect on alpha–fMRI correlations,” NeuroImage, 47, No. 1, 69–76 (2009).

    PubMed  Google Scholar 

  10. Dedovic, K., Slavich, G. M., Muscatell, K. A., et al., “Dorsal anterior cingulate cortex responses to repeated social evaluative feedback in young women with and without a history of depression,” Front. Behav. Neurosci., 10, 64–76 (2016).

    PubMed  PubMed Central  Google Scholar 

  11. Denny, B. T., Kober, H., Wager, T. D., and Ochsner, K. N., “A meta-analysis of functional neuroimaging studies of self and other judgments reveals a spatial gradient for mentalizing in medial prefrontal cortex,” J. Cogn. Neurosci., 24, No. 8, 1742–1752 (2012).

    PubMed  PubMed Central  Google Scholar 

  12. Doppelmayr, M., Klimesch, W., Hödlmoser, K., et al., “Intelligence related upper alpha desynchronization in a semantic memory task,” Brain Res. Bull., 66, No. 2, 171–177 (2005).

    CAS  PubMed  Google Scholar 

  13. Duffy, K. A., Luber, B., Adcock, R. A., and Chartrand, T. L., “Enhancing activation in the right temporoparietal junction using theta-burst stimulation: Disambiguating between two hypotheses of top-down control of behavioral mimicry,” PLoS One, 14, No. 1, e0211279 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Duncan, J., “frontal lobe function and general intelligence: why it matters,” Cortex, 41, No. 2, 215–217 (2005).

    PubMed  Google Scholar 

  15. Fox, N. A., Bakermans-Kranenburg, M. J., Yoo, K. H., et al., “Assessing human mirror activity with EEG mu rhythm: a meta-analysis,” Psychol. Bull., 142, No. 3, 291–313 (2016).

    PubMed  Google Scholar 

  16. Frenkel-Toledo, S., Bentin, S., Perry, A., et al., “Dynamics of the EEG power in the frequency and spatial domains during observation and execution of manual movements,” Brain Res., 1509, 43–57 (2013).

    CAS  PubMed  Google Scholar 

  17. Harding, I. H., Yücel, M., Harrison, B. J., et al., “Effective connectivity within the frontoparietal control network differentiates cognitive control and working memory,” NeuroImage, 106, 144–153 (2015).

    PubMed  Google Scholar 

  18. Hecht, E. E. and Parr, L. A., “The chimpanzee mirror system and the evolution of frontoparietal circuits for action observation and social learning,” in: New Frontiers in Mirror Neurons Research, Ferrari, P. and Rizzolatti, G. (eds.), Oxford University Press, Oxford (2015), pp. 153–181.

    Google Scholar 

  19. Hobson, H. M. and Bishop, D. V. M., “The interpretation of mu suppression as an index of mirror neuron activity: past, present and future,” R. Soc. Open Sci., 4, No. 3, 160662–83 (2017).

    PubMed  PubMed Central  Google Scholar 

  20. Jeon, H. and Lee, S.-H., “From neurons to social beings: Short review of the mirror neuron system research and its socio-psychological and psychiatric implications,” Clin. Psychopharmacol. Neurosci., 16, No. 1, 18–31 (2018).

    PubMed  PubMed Central  Google Scholar 

  21. Jiang, J., Borowiak, K., Tudge, L., et al., “Neural mechanisms of eye contact when listening to another person talking,” Soc. Cogn. Affect. Neurosci., 12, No. 2, 319–328 (2017).

    PubMed  Google Scholar 

  22. Kaida, A. I., Makhin, S. A., Eismont, E. V., and Pavlenko, V. B., “Developmental dynamics and topography of the individual reactivity of the EEG μ rhythm in children aged 4–14 years,” Vestn. Tomsk Gos. Univ. Biol., 45, 106–127 (2019).

    Google Scholar 

  23. Keenan, J. P., Wheeler, M. A., Gallup, G. G., and Pascual-Leone, A., “Selfrecognition and the right prefrontal cortex,” Trends Cogn. Sci., 4, No. 9, 338–344 (2000).

    CAS  PubMed  Google Scholar 

  24. Keysers, C., and Gazzola, V., “Social neuroscience: mirror neurons recorded in humans,” Curr. Biol., 20, No. 8, 353–354 (2010).

    Google Scholar 

  25. Krall, S. C., Rottschy, C., Oberwelland, E., et al., “The role of the right temporoparietal junction in attention and social interaction as revealed by ALE meta-analysis,” Brain Struct. Funct., 220, No. 2, 587–604 (2014).

    PubMed  PubMed Central  Google Scholar 

  26. Kropf, E., Syan, S. K., Minuzzi, L., and Frey, B. N., “From anatomy to function: the role of the somatosensory cortex in emotional regulation,” Braz. J. Psychiatry, 41, No. 3, 261–269 (2018).

    PubMed  PubMed Central  Google Scholar 

  27. Lago-Rodriguez, A., Cheeran, B. J., Koch, G., et al., “The role of mirror neurons in observational motor learning: an integrative review,” Eur. J. Hum. Movement, 32, 82– (2014).

    Google Scholar 

  28. Lebedeva, N. N., Karimova, E. D., Karpychev, V. V., and Mal’tsev, V. Yu., “The mirror system of the brain on observation, performance, and imagination of motor tasks – neurophysiological reflection of the perception of the consciousness of others,” Zh. Vyssh. Nerv. Deyat., 68, No. 2, 204–215 (2018).

    Google Scholar 

  29. Lebedeva, N. N., Zufman, A. I., and Mal’tsev, V. Yu., “The mirror neuron system of the brain: the key to learning, personality formation, and understanding of the consciousness of others,” Usp. Fiziol. Nauk., 48, No. 4, 16–28 (2017).

    Google Scholar 

  30. Leech, R. and Sharp, D. J., “The role of the posterior cingulate cortex in cognition and disease,” Brain, 137, No. 1, 12–32 (2014).

    PubMed  Google Scholar 

  31. Makhin, S. A., Makaricheva, A. A., Lutsyuk, N. V., and Pavlenko, V. B., “Studies of μ-rhythm reactivity on observation, auditory perception, and imitation of movements: interaction with personality properties determining empathy,” Fiziol. Cheloveka, 41, No. 6, 28–35 (2015).

    CAS  PubMed  Google Scholar 

  32. Molenberghs, P., Cunnington, R., and Mattingley, J. B., “Brain regions with mirror properties: A meta-analysis of 125 human fMRI studies,” Neurosci. Biobehav. Rev., 36, No. 1, 341–349 (2012).

    PubMed  Google Scholar 

  33. Mukamel, R., Ekstrom, A. D., Kaplan, J., et al., “Single-neuron responses in humans during execution and observation of actions,” Curr. Biol., 20, No. 8, 750–756 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Nacharova, M. A., Makhin, S. A., and Pavlenko, V. B., “Characteristics of the interaction between individual α-rhythm peak frequency and the features of general intelligence,” Uch. Zapis. Krym. Fed. Univ. im. Vernadskogo. Biol. Khim., 5, No. 2, 132–144 (2019).

    Google Scholar 

  35. Pascual-Marqui, R., “Standardized low-resolution brain electromagnetic tomography (sLORETA, technical details,” Methods Find. Exp. Clin. Pharmacol., 24, No. Suppl. D, 5–12 (2002).

  36. Paus, T., “Primate anterior cingulate cortex: where motor control, drive and cognition interface,” Nat. Rev. Neurosci., 2, No. 6, 417–424 (2001).

    CAS  PubMed  Google Scholar 

  37. Raven, J. C. and Court, J. H., Manual for Raven’s Progressive Matrices and Vocabulary Scales [Russian translation], Cogito-Center, Moscow (2012).

    Google Scholar 

  38. Raymaekers, R., Wiersema, J. R., and Roeyers, H., “EEG study of the mirror neuron system in children with high functioning autism,” Brain Res., 1304, 113–121 (2009).

    CAS  PubMed  Google Scholar 

  39. Santiesteban, I., Banissy, M. J., Catmur, C., and Bird, G., “Enhancing social ability by stimulating right temporoparietal junction,” Curr. Biol., 22, No. 23, 2274–2277 (2012).

    CAS  PubMed  Google Scholar 

  40. Saygin, A. P., “Superior temporal and premotor brain areas necessary for biological motion perception,” Brain, 130, No. 9, 2452–2461 (2007).

    PubMed  Google Scholar 

  41. Shamay-Tsoory, S. G., Tomer, R., Berger, B. D., and Aharon-Peretz, J., “Characterization of empathy defi cits following prefrontal brain damage: the role of the right ventromedial prefrontal cortex,” J. Cogn. Neurosci., 15, No. 3, 324–337 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Spengler, S., von Cramon, D. Y., and Brass, M., “Control of shared representations relies on key processes involved in mental state attribution,” Hum. Brain Mapp., 30, No. 11, 3704–3718 (2009).

    PubMed  PubMed Central  Google Scholar 

  43. Tognoli, E. and Kelso, J. A., “The coordination dynamics of social neuromarkers,” Front. Hum. Neurosci., 20, No. 9, 563–578 (2015).

    Google Scholar 

  44. Uddin, L. Q., Molnar-Szakacs, I., Zaidel, E., and Iacoboni, M., “rTMS to the right inferior parietal lobule disrupts self-other discrimination,” SCAN, 1, No. 1, 65–71 (2006).

    PubMed  Google Scholar 

  45. Varlamov, A. A., Portnova, G. V., and Makgloun, F. F., “The C-tactile system and the neurobiological mechanisms of ‘emotional’ tactile perception: discovery and current state of research,” Zh. Vyssh. Nerv. Deyat., 69, No. 3, 280–293 (2019).

    Google Scholar 

  46. Yang, J., Kitada, R., Kochiyama, T., et al., “Brain networks involved in tactile speed classification of moving dot patterns: the effects of speed and dot periodicity,” Sci. Rep., 7, 40931–40943 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  47. Zald, D. H. and Andreotti, C., “Neuropsychological assessment of the orbital and ventromedial prefrontal cortex,” Neuropsychologia, 48, No. 12, 3377–3391 (2010).

    PubMed  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to M. A. Nacharova.

Additional information

Translated from Zhurnal Vysshei Nervnoi Deyatel’nosti imeni I. P. Pavlova, Vol. 70, No. 4, pp. 446–459, July–August, 2020.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nacharova, M.A., Makhin, S.A. & Pavlenko, V.B. Localization of Sources Generating the EEG α Rhythm during Observation, Performance, and Imitation of Operant Movements in Subjects with Different Intelligence Levels. Neurosci Behav Physi 51, 182–191 (2021). https://doi.org/10.1007/s11055-021-01056-8

Download citation

Keywords

  • EEG
  • α rhythm
  • low-resolution electromagnetic tomography of the brain (sLORETA)
  • performance of movements
  • observation of movements
  • imitation of movements