Abstract
The mirror neuron system (MNS) is a brain network that has been associated with the understanding of the actions performed by others. The main areas of the brain that are considered as belonging to the MNS are the rostral part of the inferior parietal lobe (IPL) and the inferior frontal gyrus (IFG). Many studies have tried to focus on the relationship between the regions belonging to the MNS, but a little consideration has been given to the study of the MNS in resting conditions. In the present experiment, the MNS has been studied by two fMRI modalities (task-based fMRI and resting-fMRI) and three analytical procedures [task-block comparison, functional connectivity (FC), and independent component analysis (ICA)]. The task-fMRI with block design showed a mirror activity located in the rostral IPL. The coordinates of this local maximum voxel were defined as a region of interest (ROI) for an FC analysis of the resting-fMRI. This analysis revealed the existence of a functional connectivity within regions forming the core of MNS network and also with other regions with mirror properties. Finally, resting-state fMRI ICA showed the same functional network, although it was more restricted to the core MNS regions. To the best of our knowledge, this is the first study that approaches the MNS using the resting-state fMRI analysis using independent component analysis and functional connectivity at the same time.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amici S, Gorno-Tempini ML, Ogar JM et al (2006) An overview on primary progressive aphasia and its variants. Behav Neurol 17:77–87
Birn RM, Diamond JB, Smith MA, Bandettini PA (2006) Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI. Neuroimage 31:1536–1548. doi:10.1016/j.neuroimage.2006.02.048
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541
Buccino G, Binkofski F, Fink GR et al (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404
Caspers S, Geyer S, Schleicher A et al (2006) The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. Neuroimage 33:430–448. doi:10.1016/j.neuroimage.2006.06.054
Caspers S, Eickhoff SB, Geyer S et al (2008) The human inferior parietal lobule in stereotaxic space. Brain Struct Funct 212:481–495. doi:10.1007/s00429-008-0195-z
Castiello U (2005) The neuroscience of grasping. Nat Rev Neurosci 6:726–736
Cattaneo L, Rizzolatti G (2009) The mirror neuron system. Arch Neurol 66:557–560
Cohen AL, Fair DA, Dosenbach NUF et al (2008) Defining functional areas in individual human brains using resting functional connectivity MRI. Neuroimage 41:45–57. doi:10.1016/j.neuroimage.2008.01.066
Damoiseaux JS, Rombouts SARB, Barkhof F et al (2006) Consistent resting-state networks across healthy subjects. Proc Natl Acad Sci USA 103:13848–13853. doi:10.1073/pnas.0601417103
De Luca M, Beckmann CF, De Stefano N et al (2006) fMRI resting state networks define distinct modes of long-distance interactions in the human brain. Neuroimage 29:1359–1367. doi:10.1016/j.neuroimage.2005.08.035
Doucet G, Naveau M, Petit L et al (2011) Brain activity at rest: a multiscale hierarchical functional organization. J Neurophysiol 105:2753–2763. doi:10.1152/jn.00895.2010
Eickhoff SB, Stephan KE, Mohlberg H et al (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335. doi:10.1016/j.neuroimage.2004.12.034
Fazio P, Cantagallo A, Craighero L et al (2009) Encoding of human action in Broca’s area. Brain 132:1980–1988. doi:10.1093/brain/awp118
Filimon F, Nelson JD, Hagler DJ, Sereno MI (2007) Human cortical representations for reaching: mirror neurons for execution, observation, and imagery. Neuroimage 37:1315–1328. doi:10.1016/j.neuroimage.2007.06.008
Fishman I, Keown CL, Lincoln AJ et al (2014) Atypical cross talk between mentalizing and mirror neuron networks in autism spectrum disorder. JAMA Psychiatry 71:751–760. doi:10.1001/jamapsychiatry.2014.83
Fogassi L, Ferrari PF, Gesierich B et al (2005) Parietal lobe: from action organization to intention understanding. Science 308(80):662–667
Fox MD, Raichle ME (2007) Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev Neurosci 8:700–711. doi:10.1038/nrn2201
Gallese V, Fadiga L, Fogassi L, Rizzolatti G (1996) Action recognition in the premotor cortex. Brain 119(Pt 2):593–609
Gallese V, Keysers C, Rizzolatti G (2004) A unifying view of the basis of social cognition. Trends Cogn Sci 8:396–403. doi:10.1016/j.tics.2004.07.002
Gardner T, Goulden N, Cross ES (2015) Dynamic modulation of the action observation network by movement familiarity. J Neurosci 35:1561–1572. doi:10.1523/JNEUROSCI.2942-14.2015
Gazzola V, Keysers C (2009) The observation and execution of actions share motor and somatosensory voxels in all tested subjects: single-subject analyses of unsmoothed fMRI data. Cereb Cortex 19:1239–1255. doi:10.1093/cercor/bhn181
Gorno-Tempini ML, Dronkers NF, Rankin KP et al (2004) Cognition and anatomy in three variants of primary progressive aphasia. Ann Neurol 55:335–346. doi:10.1002/ana.10825
Haller S, Chapuis D, Gassert R et al (2009) Supplementary motor area and anterior intraparietal area integrate fine-graded timing and force control during precision grip. Eur J Neurosci 30:2401–2406
Himberg J, Hyvärinen A, Esposito F (2004) Validating the independent components of neuroimaging time series via clustering and visualization. Neuroimage 22:1214–1222. doi:10.1016/j.neuroimage.2004.03.027
Iacoboni M, Mazziotta JC (2007) Mirror neuron system: basic findings and clinical applications. Ann Neurol 62:213–218. doi:10.1002/ana.21198
Iacoboni M, Woods RP, Brass M et al (1999) Cortical mechanisms of human imitation. Science 286:2526–2528
Iacoboni M, Koski LM, Brass M et al (2001) Reafferent copies of imitated actions in the right superior temporal cortex. Proc Natl Acad Sci USA 98:13995–13999. doi:10.1073/pnas.241474598
Iacoboni M, Molnar-Szakacs I, Gallese V et al (2005) Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol 3:e79. doi:10.1371/journal.pbio.0030079
Igelström KM, Webb TW, Graziano MSA (2015) Neural processes in the human temporoparietal cortex separated by localized independent component analysis. J Neurosci 35:9432–9445. doi:10.1523/JNEUROSCI.0551-15.2015
Jeannerod M (2006) The origin of voluntary action: history of a physiological concept. C R Biol 329:354–362. doi:10.1016/j.crvi.2006.03.017
Jonas M, Siebner HR, Biermann-Ruben K et al (2007) Do simple intransitive finger movements consistently activate frontoparietal mirror neuron areas in humans? Neuroimage 36(Suppl 2):T44–T53
Kiviniemi V, Starck T, Remes J et al (2009) Functional segmentation of the brain cortex using high model order group PICA. Hum Brain Mapp 30:3865–3886. doi:10.1002/hbm.20813
Kokal I, Gazzola V, Keysers C (2009) Acting together in and beyond the mirror neuron system. Neuroimage 47:2046–2056. doi:10.1016/j.neuroimage.2009.06.010
Koski L, Iacoboni M, Dubeau M-C et al (2003) Modulation of cortical activity during different imitative behaviors. J Neurophysiol 89:460–471. doi:10.1152/jn.00248.2002
Lui F, Buccino G, Duzzi D et al (2008) Neural substrates for observing and imagining non-object-directed actions. Soc Neurosci 3:261–275. doi:10.1080/17470910701458551
McKeown MJ, Sejnowski TJ (1998) Independent component analysis of fMRI data: examining the assumptions. Hum Brain Mapp 6:368–372
McKeown MJ, Makeig S, Brown GG et al (1998) Analysis of fMRI data by blind separation into independent spatial components. Hum Brain Mapp 6:160–188
Mesulam MM (2001) Primary progressive aphasia. Ann Neurol 49:425–432
Molenberghs P, Cunnington R, Mattingley JB (2012) Brain regions with mirror properties: a meta-analysis of 125 human fMRI studies. Neurosci Biobehav Rev 36:341–349. doi:10.1016/j.neubiorev.2011.07.004
Mukamel R, Ekstrom AD, Kaplan J et al (2010) Single-neuron responses in humans during execution and observation of actions. Curr Biol 20:750–756. doi:10.1016/j.cub.2010.02.045
Nichols T, Brett M, Andersson J et al (2005) Valid conjunction inference with the minimum statistic. Neuroimage 25:653–660
Obrig H, Neufang M, Wenzel R et al (2000) Spontaneous low frequency oscillations of cerebral hemodynamics and metabolism in human adults. Neuroimage 12:623–639. doi:10.1006/nimg.2000.0657
Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113
Peña-Casanova J, Gramunt Fombuena N (2004) Tests neuropsicológicos. Fundamentos para una neuropsicología clínica basada en evidencias. Elsevier España S. L., Barcelona
Perry A, Stein L, Bentin S (2011) Motor and attentional mechanisms involved in social interaction—evidence from mu and alpha EEG suppression. Neuroimage 58:895–904. doi:10.1016/j.neuroimage.2011.06.060
Plata Bello J, Modroño C, Marcano F, González-Mora JL (2013) Observation of simple intransitive actions: the effect of familiarity. PLoS One 8:e74485
Plata Bello J, Modroño C, Marcano F, González-Mora JL (2014) The mirror neuron system and motor dexterity: what happens? Neuroscience 275:285–295
Rizzolatti G, Craighero L (2004) The mirror-neuron system. Annu Rev Neurosci 27:169–192. doi:10.1146/annurev.neuro.27.070203.144230
Rizzolatti G, Matelli M (2003) Two different streams form the dorsal visual system: anatomy and functions. Exp Brain Res 153:146–157. doi:10.1007/s00221-003-1588-0
Rizzolatti G, Sinigaglia C (2010) The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat Rev Neurosci 11:264–274. doi:10.1038/nrn2805
Rizzolatti G, Camarda R, Fogassi L et al (1988) Functional organization of inferior area 6 in the macaque monkey. II. Area F5 and the control of distal movements. Exp Brain Res 71:491–507
Rizzolatti G, Fogassi L, Gallese V (1997) Parietal cortex: from sight to action. Curr Opin Neurobiol 7:562–567
Rizzolatti G, Fogassi L, Gallese V (2002) Motor and cognitive functions of the ventral premotor cortex. Curr Opin Neurobiol 12:149–154
Sasaki AT, Kochiyama T, Sugiura M et al (2012) Neural networks for action representation: a functional magnetic-resonance imaging and dynamic causal modeling study. Front Hum Neurosci 6:236. doi:10.3389/fnhum.2012.00236
Schmidt RC, Fitzpatrick P, Caron R, Mergeche J (2011) Understanding social motor coordination. Hum Mov Sci 30:834–845. doi:10.1016/j.humov.2010.05.014
Schubotz RI, von Cramon DY (2004) Sequences of abstract nonbiological stimuli share ventral premotor cortex with action observation and imagery. J Neurosci 24:5467–5474. doi:10.1523/JNEUROSCI.1169-04.2004
Singer T (2012) The past, present and future of social neuroscience: a European perspective. Neuroimage 61:437–449. doi:10.1016/j.neuroimage.2012.01.109
Smith BW, Mitchell DGV, Hardin MG et al (2009) Neural substrates of reward magnitude, probability, and risk during a wheel of fortune decision-making task. Neuroimage 44:600–609. doi:10.1016/j.neuroimage.2008.08.016
Song X-W, Dong Z-Y, Long X-Y et al (2011) REST: a toolkit for resting-state functional magnetic resonance imaging data processing. PLoS One 6:e25031. doi:10.1371/journal.pone.0025031
Van Overwalle F, Baetens K (2009) Understanding others’ actions and goals by mirror and mentalizing systems: a meta-analysis. Neuroimage 48:564–584. doi:10.1016/j.neuroimage.2009.06.009
Wang L, Liu X, Guise KG et al (2010) Effective connectivity of the fronto-parietal network during attentional control. J Cogn Neurosci 22:543–553. doi:10.1162/jocn.2009.21210
Wang J, Fan L, Zhang Y et al (2012) Tractography-based parcellation of the human left inferior parietal lobule. Neuroimage 63:641–652. doi:10.1016/j.neuroimage.2012.07.045
Wheaton LA, Hallett M (2007) Ideomotor apraxia: a review. J Neurol Sci 260:1–10. doi:10.1016/j.jns.2007.04.014
Wise RG, Ide K, Poulin MJ, Tracey I (2004) Resting fluctuations in arterial carbon dioxide induce significant low frequency variations in BOLD signal. Neuroimage 21:1652–1664. doi:10.1016/j.neuroimage.2003.11.025
Zhang S, Li C-SR (2014) Functional clustering of the human inferior parietal lobule by whole-brain connectivity mapping of resting-state functional magnetic resonance imaging signals. Brain Connect 4:53–69. doi:10.1089/brain.2013.0191
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare no conflict of interest.
Ethical approval
The study was approved by the University of La Laguna Ethics Committee, according to the Declaration of Helsinki.
Informed consent
Written informed consent was explained and signed by the patients and the control subjects.
Rights and permissions
About this article
Cite this article
Plata-Bello, J., Modroño, C., Hernández-Martín, E. et al. The mirror neuron system also rests. Brain Struct Funct 222, 2193–2202 (2017). https://doi.org/10.1007/s00429-016-1335-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-016-1335-5