Brain correlates of motor complexity during observed and executed actions.
Adolescent
Adult
Brain
/ diagnostic imaging
Brain Mapping
/ instrumentation
Female
Functional Neuroimaging
/ instrumentation
Hand
Humans
Image Processing, Computer-Assisted
Male
Middle Aged
Motor Cortex
/ physiology
Motor Skills
/ physiology
Oxyhemoglobins
/ metabolism
Parietal Lobe
/ physiology
Prefrontal Cortex
/ physiology
Spectroscopy, Near-Infrared
/ instrumentation
Young Adult
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
03 07 2020
03 07 2020
Historique:
received:
05
07
2019
accepted:
05
06
2020
revised:
18
05
2020
entrez:
5
7
2020
pubmed:
6
7
2020
medline:
15
12
2020
Statut:
epublish
Résumé
Recently, cortical areas with motor properties have attracted attention widely to their involvement in both action generation and perception. Inferior frontal gyrus (IFG), ventral premotor cortex (PMv) and inferior parietal lobule (IPL), presumably consisting of motor-related areas, are of particular interest, given that they respond to motor behaviors both when they are performed and observed. Converging neuroimaging evidence has shown the functional roles of IFG, PMv and IPL in action understanding. Most studies have focused on the effects of modulations in goals and kinematics of observed actions on the brain response, but little research has explored the effects of manipulations in motor complexity. To address this, we used fNIRS to examine the brain activity in the frontal, motor, parietal and occipital regions, aiming to better understand the brain correlates involved in encoding motor complexity. Twenty-one healthy adults executed and observed two hand actions that differed in motor complexity. We found that motor complexity sensitive brain regions were present in the pars opercularis IFG/PMv, primary motor cortex (M1), IPL/supramarginal gyrus and middle occipital gyrus (MOG) during action execution, and in pars opercularis IFG/PMv and M1 during action observation. Our findings suggest that the processing of motor complexity involves not only M1 but also pars opercularis IFG, PMv and IPL, each of which plays a critical role in action perception and execution.
Identifiants
pubmed: 32620887
doi: 10.1038/s41598-020-67327-5
pii: 10.1038/s41598-020-67327-5
pmc: PMC7335074
doi:
Substances chimiques
Oxyhemoglobins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
10965Subventions
Organisme : NICHD NIH HHS
ID : P01 HD064653
Pays : United States
Organisme : Foundation for the National Institutes of Health (Foundation for the National Institutes of Health, Inc.)
ID : P41EB015896
Pays : International
Références
Casartelli, L., Molteni, M. & Ronconi, L. So close yet so far: motor anomalies impacting on social functioning in autism spectrum disorder. Neurosci. Biobehav. Rev. 63, 98–105 (2016).
pubmed: 26855233
Casartelli, L., Federici, A., Biffi, E., Molteni, M. & Ronconi, L. Are we “motorically” wired to others? High-level motor computations and their role in autism. Neuroscience https://doi.org/10.1177/1073858417750466 (2017).
doi: 10.1177/1073858417750466
Buccino, G. et al. Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Fed. Eur. Neurosci. Soc. 13, 400–404 (2001).
Buccino, G. et al. Neural circuits underlying imitation learning of hand actions: an event-related fMRI study. Neuron 42, 323–334 (2004).
pubmed: 15091346
Gazzola, V., Aziz-Zadeh, L. & Keysers, C. Empathy and the somatotopic auditory mirror system in humans. Curr. Biol. 16, 1824–1829 (2006).
pubmed: 16979560
Grafton, S. T., Arbib, M. A., Fadiga, L. & Rizzolatti, G. Localization of grasp representations in humans by positron emission tomography. Exp. Brain Res. 112, 103–111 (1996).
pubmed: 8951412
Grèzes, J., Armony, J. L., Rowe, J. & Passingham, R. E. Activations related to ‘mirror’ and ‘canonical’ neurones in the human brain: an fMRI study. Neuroimage 18, 928–937 (2003).
pubmed: 12725768
Nishitani, N. & Hari, R. Temporal dynamics of cortical representation for action. Proc. Natl. Acad. Sci. 97, 913–918 (2000).
pubmed: 10639179
Rizzolatti, G. et al. Localization of grasp representations in humans by PET: 1 Observation versus execution. Exp. Brain Res. 111, 246–252 (1996).
pubmed: 8891654
Sakreida, K. Motion class dependency in observers’ motor areas revealed by functional magnetic resonance imaging. J. Neurosci. 25, 1335–1342 (2005).
pubmed: 15703387
pmcid: 6725994
Wheaton, K. J., Thompson, J. C., Syngeniotis, A., Abbott, D. F. & Puce, A. Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. Neuroimage 22, 277–288 (2004).
pubmed: 15110018
Corbetta, M. & Shulman, G. L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 3, 201–215 (2002).
pubmed: 11994752
Price, C. J. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N. Y. Acad. Sci. 1191, 62–88 (2010).
pubmed: 20392276
Iacoboni, M. & Dapretto, M. The mirror neuron system and the consequences of its dysfunction. Nat. Rev. Neurosci. 7, 942–951 (2006).
pubmed: 17115076
Kilner, J. M. & Lemon, R. N. What we know currently about mirror neurons. Curr. Biol. 23, R1057–R1062 (2013).
pubmed: 24309286
pmcid: 3898692
Rizzolatti, G. & Fogassi, L. The mirror mechanism: recent findings and perspectives. Philos. Trans. R Soc. B Biol. Sci. 369, 20130420 (2014).
Rizzolatti, G. & Sinigaglia, C. The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations. Nat. Rev. Neurosci. 11, 264–274 (2010).
pubmed: 20216547
Rizzolatti, G. & Sinigaglia, C. The mirror mechanism: a basic principle of brain function. Nat. Rev. Neurosci. 17, 757–765 (2016).
pubmed: 27761004
Gazzola, V. et al. Aplasics born without hands mirror the goal of hand actions with their feet. Curr. Biol. 17, 1235–1240 (2007).
pubmed: 17629484
Gazzola, V., Rizzolatti, G., Wicker, B. & Keysers, C. The anthropomorphic brain: the mirror neuron system responds to human and robotic actions. Neuroimage 35, 1674–1684 (2007).
pubmed: 17395490
Lewis, J. W., Brefczynski, J. A., Phinney, R. E., Janik, J. J. & DeYoe, E. A. Distinct cortical pathways for processing tool versus animal sounds. J. Neurosci. 25, 5148–5158 (2005).
pubmed: 15917455
pmcid: 6724809
Abdollahi, R. O., Jastorff, J. & Orban, G. A. Common and segregated processing of observed actions in human SPL. Cereb. Cortex 23, 2734–2753 (2013).
pubmed: 22918981
Costantini, M., Ambrosini, E., Cardellicchio, P. & Sinigaglia, C. How your hand drives my eyes. Soc. Cogn. Affect. Neurosci. 9, 705–711 (2014).
pubmed: 23559593
Jastorff, J., Begliomini, C., Fabbri-Destro, M., Rizzolatti, G. & Orban, G. A. Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. J. Neurophysiol. 104, 128–140 (2010).
pubmed: 20445039
Peeters, R. et al. The representation of tool use in humans and monkeys: common and uniquely human features. J. Neurosci. 29, 11523–11539 (2009).
pubmed: 19759300
pmcid: 6665774
Iacoboni, M., Molnar-Szakacs, I., Gallese, V., Buccino, G. & Mazziotta, J. C. Grasping the intentions of others with one’s own mirror neuron system. PLoS Biol. 3, 0529–0535 (2005).
Molnar-Szakacs, I., Kaplan, J., Greenfield, P. M. & Iacoboni, M. Observing complex action sequences: the role of the fronto-parietal mirror neuron system. Neuroimage 33, 923–935 (2006).
pubmed: 16997576
Biagi, L., Cioni, G., Fogassi, L., Guzzetta, A. & Tosetti, M. Anterior intraparietal cortex codes complexity of observed hand movements. Brain Res. Bull. 81, 434–440 (2010).
pubmed: 20006682
Boas, D. A., Elwell, C. E., Ferrari, M. & Taga, G. Twenty years of functional near-infrared spectroscopy: introduction for the special issue. Neuroimage 85, 1–5 (2014).
pubmed: 24321364
Huppert, T. J., Hoge, R. D., Diamond, S. G., Franceschini, M. A. & Boas, D. A. A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans. Neuroimage 29, 368–382 (2006).
pubmed: 16303317
Huppert, T. J., Hoge, R. D., Dale, A. M., Franceschini, M. A. & Boas, D. A. Quantitative spatial comparison of diffuse optical imaging with blood oxygen level-dependent and arterial spin labeling-based functional magnetic resonance imaging. J. Biomed. Opt. 11, 064018 (2006).
pubmed: 17212541
pmcid: 2670188
Wijeakumar, S., Huppert, T. J., Magnotta, V. A., Buss, A. T. & Spencer, J. P. Validating an image-based fNIRS approach with fMRI and a working memory task. Neuroimage 147, 204–218 (2017).
pubmed: 27939793
Yücel, M. A., Selb, J. J., Huppert, T. J., Franceschini, M. A. & Boas, D. A. Functional near infrared spectroscopy: enabling routine functional brain imaging. Curr. Opin. Biomed. Eng. 4, 78–86 (2017).
pubmed: 29457144
pmcid: 5810962
Aasted, C. M. et al. Anatomical guidance for functional near-infrared spectroscopy: AtlasViewer tutorial. Neurophotonics 2, 020801 (2015).
pubmed: 26157991
pmcid: 4478785
Dale, A. M. Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8, 109–114 (1999).
pubmed: 10524601
pmcid: 6873302
Huppert, T. J., Diamond, S. G., Franceschini, M. A. & Boas, D. A. Hom{ER}: a review of time-series analysis methods for near-infrared spectroscopy of the brain. Appl Opt 48, D280–D298 (2009).
pubmed: 19340120
pmcid: 2761652
Jahani, S., Setarehdan, S. K., Boas, D. A. & Yücel, M. A. Motion artifact detection and correction in functional near-infrared spectroscopy: a new hybrid method based on spline interpolation method and Savitzky–Golay filtering. Neurophotonics 5, 015003 (2018).
pubmed: 29430471
pmcid: 5803523
Cope, M. & Delpy, D. T. System for long-term measurement of cerebral blood and tissue oxygenation on newborn infants by near infra-red transillumination. Med. Biol. Eng. Comput. 26(3), 289–294 (1988).
pubmed: 2855531
Delpy, D. T., Cope, M. & van der Zee, P. Estimation of optical path length through tissue from direct time of flight measurement. Phys. Med. Biol. 33, 1433–1442 (1988).
pubmed: 3237772
Boas, D. A., Dale, A. M. & Franceschini, M. A. Diffuse optical imaging of brain activation: approaches to optimizing image sensitivity, resolution, and accuracy. Neuroimage 23, S275–S288 (2004).
pubmed: 15501097
Gagnon, L. et al. Short separation channel location impacts the performance of short channel regression in NIRS. Neuroimage 59, 2518–2528 (2012).
pubmed: 21945793
Collins, D. L. et al. Design and construction of a realistic digital brain phantom. IEEE Trans. Med. Imaging 17, 463–468 (1998).
pubmed: 9735909
Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing author(s): Yoav Benjamini and Yosef Hochberg source. J. R. Stat. Soc. Ser. B 57, 289–300 (1995).
Fang, Q. Mesh-based Monte Carlo method using fast ray-tracing in Plücker coordinates. Biomed. Opt. Express 1, 165 (2010).
pubmed: 21170299
pmcid: 3003331
Arridge, S. R. Tropical review: optical tomography in medical imaging. Inverse Probl. 15, 41–93 (1999).
Boas, D. A. & Dale, A. M. Simulation study of magnetic resonance imaging-guided cortically constrained diffuse optical tomography of human brain function. Appl. Opt. 44, 1957 (2005).
pubmed: 15813532
Cooper, R. J. et al. Validating atlas-guided DOT: a comparison of diffuse optical tomography informed by atlas and subject-specific anatomies. Neuroimage 62, 1999–2006 (2012).
pubmed: 22634215
pmcid: 3408558
Bohlhalter, S. et al. Gesture subtype-dependent left lateralization of praxis planning: an event-related fMRI study. Cereb. Cortex 19, 1256–1262 (2009).
pubmed: 18796430
Fridman, E. A. et al. The role of the dorsal stream for gesture production. Neuroimage 29, 417–428 (2006).
pubmed: 16154363
Hermsdörfer, J., Terlinden, G., Mühlau, M., Goldenberg, G. & Wohlschläger, A. M. Neural representations of pantomimed and actual tool use: evidence from an event-related fMRI study. Neuroimage 36, T109–T118 (2007).
pubmed: 17499158
Johnson-Frey, S. H., Newman-Norlund, R. & Grafton, S. T. A distributed left hemisphere network active during planning of everyday tool use skills. Cereb. Cortex 15, 681–695 (2005).
pubmed: 15342430
Mäki-Marttunen, V., Villarreal, M. & Leiguarda, R. C. Lateralization of brain activity during motor planning of proximal and distal gestures. Behav. Brain Res. 272, 226–237 (2014).
pubmed: 25008350
Thoenissen, D., Zilles, K. & Toni, I. Differential involvement of parietal and precentral regions in movement preparation and motor intention. J. Neurosci. 22, 9024–9034 (2002).
pubmed: 12388609
pmcid: 6757678
Dushanova, J. & Donoghue, J. Neurons in primary motor cortex engaged during action observation. Eur. J. Neurosci. 31, 386–398 (2010).
pubmed: 20074212
pmcid: 2862560
Tkach, D., Reimer, J. & Hatsopoulos, N. G. Congruent activity during action and action observation in motor cortex. J. Neurosci. 27, 13241–13250 (2007).
pubmed: 18045918
pmcid: 6673404
Fadiga, L., Fogassi, L., Pavesi, G. & Rizzolatti, G. Motor facilitation during action observation: a magnetic stimulation study. J. Neurophysiol. 73, 2608–2611 (1995).
pubmed: 7666169
Hari, R. et al. Activation of human primary motor cortex during action observation: a neuromagnetic study. Proc. Natl. Acad. Sci. 95, 15061–15065 (1998).
pubmed: 9844015
Maeda, F., Kleiner-Fisman, G. & Pascual-Leone, A. Motor facilitation while observing hand actions: specificity of the effect and role of observer’s orientation. J. Neurophysiol. 87, 1329–1335 (2002).
pubmed: 11877507
Nishitani, N. & Hari, R. Viewing lip forms: cortical dynamics motor cortex, both during execution of hand actions. Neuron 36, 1211–1220 (2002).
pubmed: 12495633
Raos, V., Evangeliou, M. N. & Savaki, H. E. Observation of action: grasping with the mind’s hand. Neuroimage 23, 193–201 (2004).
pubmed: 15325366
Raos, V., Evangeliou, M. N. & Savaki, H. E. Mental simulation of action in the service of action perception. J. Neurosci. 27, 12675–12683 (2007).
pubmed: 18003847
pmcid: 6673334
Stefan, K. et al. Formation of a motor memory by action observation. J. Neurosci. 25, 9339–9346 (2005).
pubmed: 16221842
pmcid: 6725701
Strafella, A. P. & Paus, T. Modulation of cortical excitability during action observation: a transcranial magnetic stimulation study. Neuroreport 11, 2289 (2000).
pubmed: 10923687
Gazzola, V. & Keysers, C. 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 (2009).
pubmed: 19020203
Vigneswaran, G., Philipp, R., Lemon, R. N. & Kraskov, A. M1 corticospinal mirror neurons and their role in movement suppression during action observation. Curr. Biol. 23, 236–243 (2013).
pubmed: 23290556
pmcid: 3566480
Aziz-Zadeh, L., Koski, L., Zaidel, E., Mazziotta, J. C. & Iacoboni, M. Lateralization of the human mirror neuron system. J. Neurosci. 26, 2964–2970 (2006).
pubmed: 16540574
pmcid: 6673981
Glickstein, M. How are visual areas of the brain connected to motor areas for the sensory guidance of movement?. Trends Neurosci. 23, 613–617 (2000).
pubmed: 11137151
Wriessnegger, S. C., Kurzmann, J. & Neuper, C. Spatio-temporal differences in brain oxygenation between movement execution and imagery: a multichannel near-infrared spectroscopy study. Int. J. Psychophysiol. 67, 54–63 (2008).
pubmed: 18006099
Hanakawa, T., Dimyan, M. A. & Hallett, M. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb. Cortex 18, 2775–2788 (2008).
pubmed: 18359777
pmcid: 2583155
Koehler, S. et al. The human execution/observation matching system investigated with a complex everyday task: a functional near-infrared spectroscopy (fNIRS) study. Neurosci. Lett. 508, 73–77 (2012).
pubmed: 22206836
Yücel, M. A. et al. Short separation regression improves statistical significance and better localizes the hemodynamic response obtained by near-infrared spectroscopy for tasks with differing autonomic responses. Neurophotonics 2, 035005 (2015).
pubmed: 26835480
pmcid: 4717232