The heterogeneity of the left dorsal premotor cortex evidenced by multimodal connectivity-based parcellation and functional characterization

Genon, Sarah; Reid, Andrew; Li, Hai; Fan, Lingzhong; Müller, Veronika; Cieslik, Edna; Hoffstaedter, Felix; Langner, Robert; Grefkes, Christian; Laird, Angela; Fox, Peter; Jiang, Tianzi; Amunts, Katrin; Eickhoff, Simon

doi:10.1016/j.neuroimage.2017.02.034

Article (Scientific journals)

The heterogeneity of the left dorsal premotor cortex evidenced by multimodal connectivity-based parcellation and functional characterization

Genon, Sarah; Reid, Andrew; Li, Hai et al.

2018 • In NeuroImage, 170, p. 400-411

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https://hdl.handle.net/2268/207851

DOI
10.1016/j.neuroimage.2017.02.034

PubMed
28213119

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Abstract :

[en] Despite the common conception of the dorsal premotor cortex (PMd) as a single brain region, its diverse connectivity profiles and behavioral heterogeneity argue for a differentiated organization of the PMd. A previous study revealed that the right PMd is characterized by a rostro-caudal and a ventro-dorsal distinction dividing it into five subregions: rostral, central, caudal, ventral and dorsal. The present study assessed whether a similar organization is present in the left hemisphere, by capitalizing on a multimodal data-driven approach combining connectivity-based parcellation (CBP) based on meta-analytic modeling, resting- state functional connectivity, and probabilistic diffusion tractography. The resulting PMd modules were then characterized based on multimodal functional connectivity and a quantitative analysis of associated behavioral functions. Analyzing the clusters consistent across all modalities revealed an organization of the left PMd that mirrored its right counterpart to a large degree. Again, caudal, central and rostral modules reflected a cognitive- motor gradient and a premotor eye-field was found in the ventral part of the left PMd. In addition, a distinct module linked to abstract cognitive functions was observed in the rostro- ventral left PMd across all CBP modalities, implying greater differentiation of higher cognitive functions for the left than the right PMd.

Disciplines :

Neurosciences & behavior

Author, co-author :

Genon, Sarah ; Université de Liège > Département des sciences cliniques > Neuroimagerie des troubles de la mémoire et révalid. cogn.

Reid, Andrew

Li, Hai

Fan, Lingzhong

Müller, Veronika

Cieslik, Edna

Hoffstaedter, Felix

Langner, Robert

Grefkes, Christian

Laird, Angela

More authors (4 more)

Language :

English

Title :

The heterogeneity of the left dorsal premotor cortex evidenced by multimodal connectivity-based parcellation and functional characterization

Publication date :

15 April 2018

Journal title :

NeuroImage

ISSN :

1053-8119

eISSN :

1095-9572

Publisher :

Elsevier Science, Orlando, United States - Florida

Volume :

170

Pages :

400-411

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 03 March 2017

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356 (7 by ULiège)

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Bibliography

Abe, M., Hanakawa, T., Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex. Behav. Brain Res. 198 (2009), 13–23.
Amiez, C., Petrides, M., Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Progress. Neurobiol. 89 (2009), 220–230.
Amunts, K., Schleicher, A., Bürgel, U., Mohlberg, H., Uylings, H., Zilles, K., Broca's region revisited: cytoarchitecture and intersubject variability. J. Comp. Neurol. 412 (1999), 319–341.
Badre, D., Cognitive control, hierarchy, and the rostro-caudal organization of the frontal lobes. Trends Cogn. Sci. 12 (2008), 193–200.
Badre, D., D'Esposito, M., Is the rostro-caudal axis of the frontal lobe hierarchical?. Nat. Rev. Neurosci. 10 (2009), 659–669.
Bahlmann, J., Blumenfeld, R.S., D'Esposito, M., The rostro-caudal axis of frontal cortex is sensitive to the domain of stimulus information. Cereb. Cortex 25 (2015), 1815–1826.
Behrens, T., Berg, H.J., Jbabdi, S., Rushworth, M., Woolrich, M., Probabilistic diffusion tractography with multiple fibre orientations: what can we gain?. NeuroImage 34 (2007), 144–155.
Behrens, T.E., Woolrich, M.W., Jenkinson, M., Johansen-Berg, H., Nunes, R.G., Clare, S., Matthews, P.M., Brady, J.M., Smith, S.M., Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn. Reson. Med. 50 (2003), 1077–1088.
Tej, Behrens, Johansen-Berg, H., Woolrich, M.W., Smith, S.M., Cam, Wheeler-Kingshott, Boulby, P.A., Barker, G.J., Sillery, E.L., Sheehan, K., Ciccarelli, O., Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat. Neurosci. 6 (2003), 750-–7757.
Bellec, P., Rosa-Neto, P., Lyttelton, O.C., Benali, H., Evans, A.C., Multi-level bootstrap analysis of stable clusters in resting-state fMRI. NeuroImage 51 (2010), 1126–1139.
Birn, R.M., The role of physiological noise in resting-state functional connectivity. NeuroImage 62 (2012), 864–870.
Boussaoud, D., Attention versus intention in the primate premotor cortex. NeuroImage 14 (2001), S40–S45.
Boussaoud, D., di Pellegrino, G., Wise, S.P., Frontal lobe mechanisms subserving vision-for-action versus vision-for-perception. Behav. Brain Res 72 (1995), 1–15.
Burgess, G.C., Kandala, S., Nolan, D., Laumann, T.O., Power, J.D., Adeyemo, B., Harms, M.P., Petersen, S.E., Barch, D.M., Evaluation of denoising strategies to address motion-correlated artifacts in resting-state functional magnetic resonance imaging data from the human connectome project. Brain Connect., 2016.
Caspers, S., Geyer, S., Schleicher, A., Mohlberg, H., Amunts, K., Zilles, K., The human inferior parietal cortex: cytoarchitectonic parcellation and interindividual variability. NeuroImage 33 (2006), 430–448.
Caspers, S., Zilles, K., Laird, A.R., Eickhoff, S.B., ALE meta-analysis of action observation and imitation in the human brain. NeuroImage 50 (2010), 1148–1167.
Cieslik, E.C., Seidler, I., Laird, A.R., Fox, P.T., Eickhoff, S.B., Different involvement of subregions within dorsal premotor and medial frontal cortex for pro- and antisaccades. Neurosci. Biobehav. Rev. 68 (2016), 256–269.
Cieslik, E.C., Zilles, K., Caspers, S., Roski, C., Kellermann, T.S., Jakobs, O., Langner, R., Laird, A.R., Fox, P.T., Eickhoff, S.B., Is there “One” DLPFC in cognitive action control? evidence for heterogeneity from co-activation-based parcellation. Cereb. Cortex 23 (2013), 2677–2689.
Clos, M., Amunts, K., Laird, A.R., Fox, P.T., Eickhoff, S.B., Tackling the multifunctional nature of Broca's region meta-analytically: co-activation-based parcellation of area 44. NeuroImage 83 (2013), 174–188.
De Schotten, M.T., Dell'Acqua, F., Forkel, S.J., Simmons, A., Vergani, F., Murphy, D.G., Catani, M., A lateralized brain network for visuospatial attention. Nat. Neurosci. 14 (2011), 1245–1246.
Diedrichsen, J., Balsters, J.H., Flavell, J., Cussans, E., Ramnani, N., A probabilistic MR atlas of the human cerebellum. NeuroImage 46 (2009), 39–46.
Eickhoff, S.B., Amunts, K., Mohlberg, H., Zilles, K., The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results. Cereb. Cortex 16 (2006), 268–279.
Eickhoff, S.B., Bzdok, D., Laird, A.R., Kurth, F., Fox, P.T., Activation likelihood estimation meta-analysis revisited. NeuroImage 59 (2012), 2349–2361.
Eickhoff, S.B., Bzdok, D., Laird, A.R., Roski, C., Caspers, S., Zilles, K., Fox, P.T., Co-activation patterns distinguish cortical modules, their connectivity and functional differentiation. NeuroImage 57 (2011), 938–949.
Eickhoff, S.B., Stephan, K.E., Mohlberg, H., Grefkes, C., Fink, G.R., Amunts, K., Zilles, K., A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. NeuroImage 25 (2005), 1325–1335.
Eickhoff, S.B., Thirion, B., Varoquaux, G., Bzdok, D., Connectivity-based parcellation: critique and implications. Human. brain Mapp. 36 (2015), 4771–4792.
Foster, B.L., He, B.J., Honey, C.J., Jerbi, K., Maier, A., Saalmann, Y.B., Spontaneous neural dynamics and multi-scale network organization. Front. Syst. Neurosci., 10, 2016, 7.
Genon, S., Li, H., Fan, L., Muller, V.I., Cieslik, E.C., Hoffstaedter, F., Reid, A.T., Langner, R., Grefkes, C., Fox, P.T., Moebus, S., Caspers, S., Amunts, K., Jiang, T., Eickhoff, S.B., The right dorsal premotor mosaic: organization, functions, and connectivity. Cereb. Cortex, 2016.
Geyer, S., Ledberg, A., Schleicher, A., Kinomura, S., Schormann, T., Burgel, U., Klingberg, T., Larsson, J., Zilles, K., Roland, P.E., Two different areas within the primary motor cortex of man. Nature 382 (1996), 805–807.
Geyer, S., Matelli, M., Luppino, G., Zilles, K., Functional neuroanatomy of the primate isocortical motor system. Anat. Embryol. 202 (2000), 443–474.
Geyer, S., Schleicher, A., Zilles, K., Areas 3a, 3b, and 1 of human primary somatosensory cortex. NeuroImage 10 (1999), 63–83.
Glasser, M., Coalson, T., Robinson, E., Hacker, C., Harwell, J., Yacoub, E., Ugurbil, K., Anderson, J., Beckmann, C., Jenkinson, M., A Multi-modal parcellation of human cerebral cortex. Nature, 2016.
Grefkes, C., Geyer, S., Schormann, T., Roland, P., Zilles, K., Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. NeuroImage 14 (2001), 617–631.
Griffanti, L., Salimi-Khorshidi, G., Beckmann, C.F., Auerbach, E.J., Douaud, G., Sexton, C.E., Zsoldos, E., Ebmeier, K.P., Filippini, N., Mackay, C.E., Moeller, S., Xu, J., Yacoub, E., Baselli, G., Ugurbil, K., Miller, K.L., Smith, S.M., ICA-based artefact removal and accelerated fMRI acquisition for improved resting state network imaging. NeuroImage 95 (2014), 232–247.
Grosbras, M.H., Beaton, S., Eickhoff, S.B., Brain regions involved in human movement perception: a quantitative voxel-based meta-analysis. Human. brain Mapp. 33 (2012), 431–454.
Gross, C.G., How inferior temporal cortex became a visual area. Cereb. Cortex 4 (1994), 455–469.
Hanakawa, T., Rostral premotor cortex as a gateway between motor and cognitive networks. Neurosci. Res. 70 (2011), 144–154.
Hardwick, R.M., Rottschy, C., Miall, R.C., Eickhoff, S.B., A quantitative meta-analysis and review of motor learning in the human brain. NeuroImage 67 (2013), 283–297.
Hoshi, E., Tanji, J., Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties. Curr. Opin. Neurobiol. 17 (2007), 234–242.
Kantak, S.S., Stinear, J.W., Buch, E.R., Cohen, L.G., Rewiring the brain: potential role of the premotor cortex in motor control, learning, and recovery of function following brain injury. Neurorehabilitation Neural Repair 26 (2012), 282–292.
Kell, C., Morillon, B., Kouneiher, F., Giraud A., 2010. Lateralization of speech production starts in sensory cortices—a possible sensory origin of cerebral left dominance for speech. Cerebral Cortex:bhq167.
Koechlin, E., Summerfield, C., An information theoretical approach to prefrontal executive function. Trends Cogn. Sci. 11 (2007), 229–235.
Laird, A.R., Eickhoff, S.B., Kurth, F., Fox, P.M., Uecker, A.M., Turner, J.A., Robinson, J.L., Lancaster, J.L., Fox, P.T., ALE meta-analysis workflows via the brainmap database: progress towards a probabilistic functional brain atlas. Front. neuroinformatics, 3, 2009.
Langner, R., Eickhoff, S.B., Sustaining attention to simple tasks: a meta-analytic review of the neural mechanisms of vigilant attention. Psychol. Bull. 139 (2013), 870–900.
Laumann, T.O., Gordon, E.M., Adeyemo, B., Snyder, A.Z., Joo, S.J., Chen, M.Y., Gilmore, A.W., McDermott, K.B., Nelson, S.M., Dosenbach, N.U., Schlaggar, B.L., Mumford, J.A., Poldrack, R.A., Petersen, S.E., Functional system and areal organization of a highly sampled individual human brain. Neuron 87 (2015), 657–670.
Lebedev, M.A., Wise, S.P., Tuning for the orientation of spatial attention in dorsal premotor cortex. Eur. J. Neurosci. 13 (2001), 1002–1008.
Luppino, G., Rozzi, S., Calzavara, R., Matelli, M., Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur. J. Neurosci. 17 (2003), 559–578.
Matelli, M., Luppino, G., Rizzolatti, G., Patterns of cytochrome oxidase activity in the frontal agranular cortex of the macaque monkey. Behav. brain Res. 18 (1985), 125–136.
Matelli, M., Luppino, G., Rizzolatti, G., Architecture of superior and mesial area 6 and the adjacent cingulate cortex in the macaque monkey. J. Comp. Neurol. 311 (1991), 445–462.
Morosan, P., Schleicher, A., Amunts, K., Zilles, K., Multimodal architectonic mapping of human superior temporal gyrus. Anat. Embryol. (Berl.) 210 (2005), 401–406.
Murphy, K., Birn, R.M., Bandettini, P.A., Resting-state fMRI confounds and cleanup. NeuroImage 80 (2013), 349–359.
Nakayama, Y., Yamagata, T., Hoshi, E., Rostrocaudal functional gradient among the pre-dorsal premotor cortex, dorsal premotor cortex and primary motor cortex in goal-directed motor behaviour. Eur. J. Neurosci. 43 (2016), 1569–1589.
Orban, P., Doyon, J., Petrides, M., Mennes, M., Hoge, R., Bellec, P., The richness of task-evoked hemodynamic responses defines a pseudohierarchy of functionally meaningful brain networks. Cereb. Cortex 25 (2015), 2658–2669.
Picard, N., Strick, P.L., Imaging the premotor areas. Curr. Opin. Neurobiol. 11 (2001), 663–672.
Reid, A.T., Bzdok, D., Genon, S., Langner, R., Muller, V.I., Eickhoff, C.R., Hoffstaedter, F., Cieslik, E.C., Fox, P.T., Laird, A.R., Amunts, K., Caspers, S., Eickhoff, S.B., ANIMA: a data-sharing initiative for neuroimaging meta-analyses. NeuroImage 124 (2016), 1245–1253.
Rizzolatti, G., Luppino, G., The cortical motor system. Neuron 31 (2001), 889–901.
Rothstein, H.R., Sutton, A.J., Borenstein, M., Publication Bias in Meta-Analysis. 2006, Publication Bias in Meta-Analysis John Wiley & Sons, Ltd, 1–7.
Rottschy, C., Caspers, S., Roski, C., Reetz, K., Dogan, I., Schulz, J.B., Zilles, K., Laird, A.R., Fox, P.T., Eickhoff, S.B., Differentiated parietal connectivity of frontal regions for “what” and “where” memory. Brain Struct. Funct. 218 (2013), 1551–1567.
Rottschy, C., Langner, R., Dogan, I., Reetz, K., Laird, A.R., Schulz, J.B., Fox, P.T., Eickhoff, S.B., Modelling neural correlates of working memory: a coordinate-based meta-analysis. NeuroImage 60 (2012), 830–846.
Salimi-Khorshidi, G., Douaud, G., Beckmann, C.F., Glasser, M.F., Griffanti, L., Smith, S.M., Automatic denoising of functional MRI data: combining independent component analysis and hierarchical fusion of classifiers. NeuroImage 90 (2014), 449–468.
Scheperjans, F., Eickhoff, S.B., Homke, L., Mohlberg, H., Hermann, K., Amunts, K., Zilles, K., Probabilistic maps, morphometry, and variability of cytoarchitectonic areas in the human superior parietal cortex. Cereb. Cortex 18 (2008), 2141–2157.
Schubotz, R.I., Anwander, A., Knösche, T.R., von Cramon, D.Y., Tittgemeyer, M., Anatomical and functional parcellation of the human lateral premotor cortex. NeuroImage 50 (2010), 396–408.
Sigl, B., Caspers, S., Mohlberg, H., Cieslik, E., Eickhoff, S., Amunts, K., 2016. The human dorsal premotor cortex–cytoarchitecture, maps and function. Proceedings of the OHBM 2016 Annual Meeting.
Van Essen, D.C., Jbabdi, S., Sotiropoulos, S.N., Chen, C., Dikranian, K., Coalson, T., Harwell, J., Behrens, T.E., Glasser, M.F. 2013. Mapping connections in humans and nonhuman primates: aspirations and challenges for diffusion imaging. Diffusion MRI, 2nd edition (eds Johansen-Berg, H., Behrens, T.E.J.):337—358.
Vossel, S., Geng, J.J., Fink, G.R., Dorsal and ventral attention systems distinct neural circuits but collaborative roles. Neuroscientist 20 (2014), 150–159.
Wager, T.D., Jonides, J., Reading, S., Neuroimaging studies of shifting attention: a meta-analysis. NeuroImage 22 (2004), 1679–1693.
Yeo, B.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., Roffman, J.L., Smoller, J.W., Zöllei, L., Polimeni, J.R., The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106 (2011), 1125–1165.
Yeo, B.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., Roffman, J.L., Smoller, J.W., Zollei, L., Polimeni, J.R., Fischl, B., Liu, H., Buckner, R.L., The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol. 106 (2011), 1125–1165.
Yeo, B.T.T., Krienen, F.M., Sepulcre, J., Sabuncu, M.R., Lashkari, D., Hollinshead, M., Roffman, J.L., Smoller, J.W., Zöllei, L., Polimeni, J.R., The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J. Neurophysiol. 106 (2011), 1125–1165.