Wrist and finger motor representations embedded in the cerebral and cerebellar resting-state activation.
Cerebellum
Cross-decoding
Resting state
Sensorimotor cortex
Somatotopy
fMRI
Journal
Brain structure & function
ISSN: 1863-2661
Titre abrégé: Brain Struct Funct
Pays: Germany
ID NLM: 101282001
Informations de publication
Date de publication:
Sep 2021
Sep 2021
Historique:
received:
02
11
2020
accepted:
22
06
2021
pubmed:
9
7
2021
medline:
27
1
2022
entrez:
8
7
2021
Statut:
ppublish
Résumé
Several functional magnetic resonance imaging (fMRI) studies have demonstrated that resting-state brain activity consists of multiple components, each corresponding to the spatial pattern of brain activity induced by performing a task. Especially in a movement task, such components have been shown to correspond to the brain activity pattern of the relevant anatomical region, meaning that the voxels of pattern that are cooperatively activated while using a body part (e.g., foot, hand, and tongue) also behave cooperatively in the resting state. However, it is unclear whether the components involved in resting-state brain activity correspond to those induced by the movement of discrete body parts. To address this issue, in the present study, we focused on wrist and finger movements in the hand, and a cross-decoding technique trained to discriminate between the multi-voxel patterns induced by wrist and finger movement was applied to the resting-state fMRI. We found that the multi-voxel pattern in resting-state brain activity corresponds to either wrist or finger movements in the motor-related areas of each hemisphere of the cerebrum and cerebellum. These results suggest that resting-state brain activity in the motor-related areas consists of the components corresponding to the elementary movements of individual body parts. Therefore, the resting-state brain activity possibly has a finer structure than considered previously.
Identifiants
pubmed: 34236531
doi: 10.1007/s00429-021-02330-8
pii: 10.1007/s00429-021-02330-8
pmc: PMC8354910
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2307-2319Subventions
Organisme : Brain/MINDS from AMED
ID : 21dm0207070h0003
Organisme : Brain/MINDS from AMED
ID : 21dm0307003h0004
Organisme : KAKENHI from JSPS
ID : 26870934
Organisme : KAKENHI from JSPS
ID : 26120008
Organisme : KAKENHI from JSPS
ID : 18H04960
Organisme : KAKENHI from JSPS
ID : 16H03306
Organisme : KAKENHI from JSPS
ID : 19H03536
Organisme : KAKENHI from JSPS
ID : 17H02128
Commentaires et corrections
Type : ErratumIn
Informations de copyright
© 2021. The Author(s).
Références
Albert NB, Robertson EM, Miall RC (2009) The resting human brain and motor learning. Curr Biol 19:1023–1027 (Elsevier)
pubmed: 19427210
pmcid: 2701987
doi: 10.1016/j.cub.2009.04.028
Amunts K et al (2007) Gender-specific left–right asymmetries in human visual cortex. J Neurosci (soc Neurosci) 27:1356–1364
doi: 10.1523/JNEUROSCI.4753-06.2007
Amunts K, Schleicher A, Zilles K (2007) Cytoarchitecture of the cerebral cortex—more than localization. Neuroimage 37:1061–1065 (Elsevier)
pubmed: 17870622
doi: 10.1016/j.neuroimage.2007.02.037
Arbabshirani MR, Havlicek M, Kiehl KA, Pearlson GD, Calhoun VD (2013) Functional network connectivity during rest and task conditions: a comparative study. Hum Brain Mapp 34:2959–2971 (Wiley Online Library)
pubmed: 22736522
doi: 10.1002/hbm.22118
Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995) Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Resonan Med 34:537–541 (Wiley Subscription Services, Inc., A Wiley Company)
doi: 10.1002/mrm.1910340409
Biswal B, Deyoe EA, Hyde JS (1996) Reduction of physiological fluctuations in fMRI using digital filters. Magn Reson Med 35:107–113 (Wiley Online Library)
pubmed: 8771028
doi: 10.1002/mrm.1910350114
Brett M, Anton J-L, Valabregue R, Poline J-B (2002) Region of interest analysis using the MarsBar toolbox for SPM 99. Neuroimage 16:S497
Buccino G et al (2001) Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study. Eur J Neurosci 13:400–404 (Wiley Online Library)
pubmed: 11168545
Bundy DT, Wronkiewicz M, Sharma M, Moran DW, Corbetta M, Leuthardt EC (2012) Using ipsilateral motor signals in the unaffected cerebral hemisphere as a signal platform for brain–computer interfaces in hemiplegic stroke survivors. J Neural Eng 9:36011 (IOP Publishing)
doi: 10.1088/1741-2560/9/3/036011
Davis T, LaRocque KF, Mumford JA, Norman KA, Wagner AD, Poldrack RA (2014) What do differences between multi-voxel and univariate analysis mean? How subject-, voxel-, and trial-level variance impact fMRI analysis. Neuroimage 97:271–283 (Elsevier)
pubmed: 24768930
doi: 10.1016/j.neuroimage.2014.04.037
Deuker et al (2013) Memory consolidation by replay of stimulus-specific neural activity. J Neurosci (soc Neurosci) 33:19373–19383
doi: 10.1523/JNEUROSCI.0414-13.2013
Di X, Gohel S, Kim EH, Biswal BB (2013) Task vs rest—different network configurations between the coactivation and the resting-state brain networks. Front Hum Neurosci (front) 7:493
Diedrichsen J, Wiestler T, Krakauer JW (2012) Two distinct ipsilateral cortical representations for individuated finger movements. Cereb Cortex 23:1362–1377 (Oxford University Press)
pubmed: 22610393
pmcid: 3643717
doi: 10.1093/cercor/bhs120
Fischl B (2012) FreeSurfer. Neuroimage 62:774–781 ((Elsevier))
pubmed: 22248573
doi: 10.1016/j.neuroimage.2012.01.021
Fischl B et al (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355 (Elsevier)
pubmed: 11832223
doi: 10.1016/S0896-6273(02)00569-X
Fischl B et al (2007) Cortical folding patterns and predicting cytoarchitecture. Cerebr Cortex 18:1973–1980 (Oxford University Press)
doi: 10.1093/cercor/bhm225
Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, Raichle ME (2005) The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proc Natl Acad Sci USA (natl Acad Sci) 102:9673–9678
doi: 10.1073/pnas.0504136102
Fujiwara Y et al (2017) eural pattern similarity between contra-and ipsilateral movements in high-frequency band of human electrocorticograms. Neuroimage 147:302–313 (Elsevier)
pubmed: 27890491
doi: 10.1016/j.neuroimage.2016.11.058
Genon S et al (2017) The right dorsal premotor mosaic: organization, functions, and connectivity. Cerebr Cortex 27:2095–2110 (Oxford University Press)
Genon S et al (2018) The heterogeneity of the left dorsal premotor cortex evidenced by multimodal connectivity-based parcellation and functional characterization. Neuroimage 170:400–411 (Elsevier)
pubmed: 28213119
doi: 10.1016/j.neuroimage.2017.02.034
Grefkes C et al (2008) Cortical connectivity after subcortical stroke assessed with functional magnetic resonance imaging. Ann Neurol 63:236–246 (Wiley Online Library)
pubmed: 17896791
doi: 10.1002/ana.21228
Greicius MD, Srivastava G, Reiss AL, Menon V (2004) Default-mode network activity distinguishes Alzheimerś disease from healthy aging: evidence from functional MRI. Proc Natl Acad Sci USA (natl Acad Sci) 101:4637–4642
doi: 10.1073/pnas.0308627101
Grodd W, Hülsmann E, Lotze M, Wildgruber D, Erb M (2001) Sensorimotor mapping of the human cerebellum: fMRI evidence of somatotopic organization. Hum Brain Mapp 13:55–73 (Wiley Online Library)
pubmed: 11346886
pmcid: 6871814
doi: 10.1002/hbm.1025
Guidotti R, Del Gratta C, Baldassarre A, Romani GL, Corbetta M (2015) Visual learning induces changes in resting-state fMRI multivariate pattern of information. J Neurosci (soc Neurosci) 35:9786–9798
doi: 10.1523/JNEUROSCI.3920-14.2015
Haynes J-D, Rees G (2005a) Predicting the orientation of invisible stimuli from activity in human primary visual cortex. Nat Neurosci 8:686–691 (Nature Publishing Group)
pubmed: 15852013
doi: 10.1038/nn1445
Haynes J-D, Rees G (2005b) Predicting the stream of consciousness from activity in human visual cortex. Curr Biol 15:1301–1307 (Nature Publishing Group)
pubmed: 16051174
doi: 10.1016/j.cub.2005.06.026
Hinds OP et al (2008) Accurate prediction of V1 location from cortical folds in a surface coordinate system. Neuroimage 39:1585–1599 (Elsevier)
pubmed: 18055222
doi: 10.1016/j.neuroimage.2007.10.033
Hoshiyama M et al (1997) Identification of motor and sensory brain activities during unilateral finger movement: spatiotemporal source analysis of movement-associated magnetic fields. Exp Brain Res 115:6–14 (Springer)
pubmed: 9224829
doi: 10.1007/PL00005685
Hotson G et al (2014) Coarse electrocorticographic decoding of ipsilateral reach in patients with brain lesions. PLoS ONE 9:e115236 (Public Library of Science)
pubmed: 25545500
pmcid: 4278860
doi: 10.1371/journal.pone.0115236
Kamitani Y, Tong F (2005) Decoding the visual and subjective contents of the human brain. Nat Neurosci 8:679–685 (Nature Publishing Group)
pubmed: 15852014
pmcid: 1808230
doi: 10.1038/nn1444
Kamitani Y, Tong F (2006) Decoding seen and attended motion directions from activity in the human visual cortex. Curr Biol 16:1096–1102 (Elsevier)
pubmed: 16753563
pmcid: 1635016
doi: 10.1016/j.cub.2006.04.003
Kenet T, Bibitchkov D, Tsodyks M, Grinvald A, Arieli A (2003) Spontaneously emerging cortical representations of visual attributes. Nature 425:954–956 (Nature Publishing Group)
pubmed: 14586468
doi: 10.1038/nature02078
Kobayashi M, Hutchinson S, Schlaug G, Pascual-Leone A (2003) Ipsilateral motor cortex activation on functional magnetic resonance imaging during unilateral hand movements is related to interhemispheric interactions. Neuroimage 20:2259–2270 (Elsevier)
pubmed: 14683727
doi: 10.1016/S1053-8119(03)00220-9
Kriegeskorte N (2011) Pattern-information analysis: from stimulus decoding to computational-model testing. Neuroimage 56:411–421 (Elsevier)
pubmed: 21281719
doi: 10.1016/j.neuroimage.2011.01.061
Kurashige H, Yamashita Y, Hanakawa T, Honda M (2018) A knowledge-based arrangement of prototypical neural representation prior to experience contributes to selectivity in upcoming knowledge acquisition. Front Hum Neurosci (front) 12:111
doi: 10.3389/fnhum.2018.00111
Laird AR et al (2011) Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci 23:4022–4037 (MIT Press)
pubmed: 21671731
pmcid: 3690655
doi: 10.1162/jocn_a_00077
Lee MH, Smyser CD, Shimony JS (2013) Resting-state fMRI: a review of methods and clinical applications. Am J Neuroradiol (am Soc Neuroradiol) 34:1866–1872
doi: 10.3174/ajnr.A3263
Liu Y et al (2010) Decoding ipsilateral finger movements from ecog signals in humans. Adv Neural Inf Process Syst 1468–1476
Long X, Goltz D, Margulies DS, Nierhaus T, Villringer A (2014) Functional connectivity-based parcellation of the human sensorimotor cortex. Eur J Neurosci 39:1332–1342 (Wiley Online Library)
pubmed: 24417550
doi: 10.1111/ejn.12473
Lotze M et al (1999) Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosci 11:491–501 (MIT Press)
pubmed: 10511638
doi: 10.1162/089892999563553
Lu K-H, Jeong JY, Wen H, Liu Z (2017) Spontaneous activity in the visual cortex is organized by visual streams. Hum Brain Mapp 38:4613–4630 (Wiley Online Library)
pubmed: 28608643
pmcid: 5546954
doi: 10.1002/hbm.23687
Luczak A, Barthó P, Harris KD (2009) Spontaneous events outline the realm of possible sensory responses in neocortical populations. Neuron 62:413–425 (Elsevier)
pubmed: 19447096
pmcid: 2696272
doi: 10.1016/j.neuron.2009.03.014
Manni E, Petrosini L (2004) A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 5:241–249 (Nature Publishing Group)
pubmed: 14976523
doi: 10.1038/nrn1347
Meier JD, Aflalo TN, Kastner S, Graziano MSA (2008) Complex organization of human primary motor cortex: a high-resolution fMRI study. J Neurophysiol (am Physiol Soc) 100:1800–1812
doi: 10.1152/jn.90531.2008
Miyawaki Y et al (2008) Visual image reconstruction from human brain activity using a combination of multiscale local image decoders. Neuron 60:915–929 (Elsevier)
pubmed: 19081384
doi: 10.1016/j.neuron.2008.11.004
Mullinger KJ, Mayhew SD, Bagshaw AP, Bowtell R, Francis ST (2014) Evidence that the negative BOLD response is neuronal in origin: a simultaneous EEG–BOLD–CBF study in humans. Neuroimage 94:263–274 (Elsevier)
pubmed: 24632092
doi: 10.1016/j.neuroimage.2014.02.029
Newton JM, Sunderland A, Gowland PA (2005) fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement. Neuroimage 24:1080–1087 (Elsevier)
pubmed: 15670685
doi: 10.1016/j.neuroimage.2004.10.003
Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10:424–430 (Elsevier)
pubmed: 16899397
doi: 10.1016/j.tics.2006.07.005
Ogawa K, Imamizu H (2013) Human sensorimotor cortex represents conflicting visuomotor mappings. J Neurosci (soc Neurosci) 33:6412–6422
doi: 10.1523/JNEUROSCI.4661-12.2013
Ogawa S, Lee T-M, Kay AR, Tank DW (1990) Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci (natl Acad Sci) 87:9868–9872
doi: 10.1073/pnas.87.24.9868
Penfield W, Rasmussen T (1952) The cerebral cortex of man. MacMillan Company, New York
Penny WD, Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE (2011) Statistical parametric mapping: the analysis of functional brain images: the analysis of functional brain images. Academic press, Cambridge
Raichle ME (2010) Two views of brain function. Trends Cogn Sci 14:180–190 (Elsevier)
pubmed: 20206576
doi: 10.1016/j.tics.2010.01.008
Rehme AK, Grefkes C (2013) Cerebral network disorders after stroke: evidence from imaging-based connectivity analyses of active and resting brain states in humans. J Physiol 591:17–31 (Wiley Online Library)
pubmed: 23090951
doi: 10.1113/jphysiol.2012.243469
Rehme AK, Eickhoff SB, Grefkes C (2013) State-dependent differences between functional and effective connectivity of the human cortical motor system. Neuroimage 67:237–246 (Elsevier)
pubmed: 23201364
doi: 10.1016/j.neuroimage.2012.11.027
Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31:889–901 (Elsevier)
pubmed: 11580891
doi: 10.1016/S0896-6273(01)00423-8
Satterthwaite TD et al (2013) An improved framework for confound regression and filtering for control of motion artifact in the preprocessing of resting-state functional connectivity data. Neuroimage 64:240–256
pubmed: 22926292
doi: 10.1016/j.neuroimage.2012.08.052
Schapiro AC, McDevitt EA, Rogers TT, Mednick SC, Norman KA (2018) Human hippocampal replay during rest prioritizes weakly learned information and predicts memory performance. Nat Commun 9:3920 (Nature Publishing Group)
pubmed: 30254219
pmcid: 6156217
doi: 10.1038/s41467-018-06213-1
Scherer R, Zanos SP, Miller KJ, Rao RPN, Ojemann JG (2009) Classification of contralateral and ipsilateral finger movements for electrocorticographic brain–computer interfaces. Neurosurg Focus (am Assoc Neurol Surg) 27:12
doi: 10.3171/2009.4.FOCUS0981
Schieber MH (2001) Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol (am Physiol Soc Bethesda, MD) 86:2125–2143
Schomburg A, Venema V, Ament F, Simmer C (2012) Application of an adaptive radiative transfer scheme in a mesoscale numerical weather prediction model. Q J R Meteorol Soc 138:91–102 (Wiley Online Library)
doi: 10.1002/qj.890
Sheline YI, Raichle ME (2013) Resting state functional connectivity in preclinical Alzheimerś disease. Biol Psychiatry 74:340–347 (Elsevier)
pubmed: 23290495
pmcid: 3537262
doi: 10.1016/j.biopsych.2012.11.028
Smith SM (2002) Fast robust automated brain extraction. Human Brain Mapp 17:143–155
doi: 10.1002/hbm.10062
Smith SM et al (2004) Advances in functional and structural MR image analysis and implementation as FSL. Neuroimage 23:S208–S219 ((Elsevier))
pubmed: 15501092
doi: 10.1016/j.neuroimage.2004.07.051
Smith SM et al (2009) Correspondence of the brainś functional architecture during activation and rest. Proc Natl Acad Sci (natl Acad Sci) 106:13040–13045
doi: 10.1073/pnas.0905267106
Tanji J, Okano K, Sato KC (1988) Neuronal activity in cortical motor areas related to ipsilateral, contralateral, and bilateral digit movements of the monkey. J Neurophysiol (am Physiol Soc) 60:325–343
doi: 10.1152/jn.1988.60.1.325
Toga AW, Thompson PM, Mori S, Amunts K, Zilles K (2006) Towards multimodal atlases of the human brain. Nat Rev Neurosci (nature Publishing Group) 7:952
doi: 10.1038/nrn2012
Van Meer MP et al (2010) Recovery of sensorimotor function after experimental stroke correlates with restoration of resting-state interhemispheric functional connectivity. J Neurosci (soc Neurosci) 30:3964–3972
doi: 10.1523/JNEUROSCI.5709-09.2010
Venema V et al (2006) Surrogate cloud fields generated with the iterative amplitude adapted Fourier transform algorithm. Tellus A 58:104–120 (Wiley Online Library)
doi: 10.1111/j.1600-0870.2006.00160.x
Venema V, Schomburg A, Ament F, Simmer C (2007) Two adaptive radiative transfer schemes for numerical weather prediction models. Atmos Chem Phys (copernicus GmbH) 7:5659–5674
doi: 10.5194/acp-7-5659-2007
Verstynen T, Ivry RB (2011) Network dynamics mediating ipsilateral motor cortex activity during unimanual actions. J Cogn Neurosci 23:2468–2480 (MIT Press)
pubmed: 21268666
doi: 10.1162/jocn.2011.21612
Verstynen T, Diedrichsen J, Albert N, Aparicio P, Ivry RB (2005) Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. J Neurophysiol (am Physiol Soc) 93:1209–1222
doi: 10.1152/jn.00720.2004
Walther DB, Chai B, Caddigan E, Beck DM, Fei-Fei Li (2011) Simple line drawings suffice for functional MRI decoding of natural scene categories. Proc Natl Acad Sci (natl Acad Sci) 108:9661–9666
doi: 10.1073/pnas.1015666108
Wang L, Shen H, Tang F, Zang Y, Dewen Hu (2012) Combined structural and resting-state functional MRI analysis of sexual dimorphism in the young adult human brain: an MVPA approach. Neuroimage (elsevier) 61:931–940
doi: 10.1016/j.neuroimage.2012.03.080
Wang Z et al (2013) The relationship of anatomical and functional connectivity to resting-state connectivity in primate somatosensory cortex. Neuron 78:1116–1126
pubmed: 23791200
pmcid: 3723346
doi: 10.1016/j.neuron.2013.04.023
Wilcoxon F (1945) Individual comparisons by ranking methods. Biometr Bull (JSTOR) 1:80–83
doi: 10.2307/3001968
Wilf M, Strappini F, Golan T, Hahamy A, Harel M, Malach R (2017) Spontaneously emerging patterns in human visual cortex reflect responses to naturalistic sensory stimuli. Cerebr Cortex 27:750–763 (Oxford University Press)
Woolsey CN, Erickson TC, Gilson WE (1979) Localization in somatic sensory and motor areas of human cerebral cortex as determined by direct recording of evoked potentials and electrical stimulation. J Neurosurg (j NeurosuRg Publishing Group) 51:476–506
Yamashita O (2011) SLR Toolbox Web Page
Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002) Quantitative analysis of cyto-and receptor architecture of the human brain. Brain mapping: the methods. Elsevier, Amsterdam, pp 573–602
doi: 10.1016/B978-012693019-1/50023-X