Science - USA (2021-11-12)

(Antfer) #1

  1. L. Cardinaliet al., Tool-use induces morphological updating of
    the body schema.Curr. Biol. 19 , R478–R479 (2009).
    doi:10.1016/j.cub.2009.06.048; pmid: 19549491

  2. M. Jeannerod, Visuomotor channels: Their integration in
    goal-directed prehension.Hum. Mov. Sci. 18 , 201–218 (1999).
    doi:10.1016/S0167-9457(99)00008-1

  3. L. Cardinali, C. Brozzoli, L. Finos, A. C. Roy, A. Farnè, The rules
    of tool incorporation: Tool morpho-functional & sensori-motor
    constraints.Cognition 149 ,1–5 (2016). doi:10.1016/
    j.cognition.2016.01.001; pmid: 26774102

  4. Y. Itaguchi, K. Fukuzawa, Hand-use and tool-use in grasping
    control.Exp. Brain Res. 232 , 3613–3622 (2014). doi:10.1007/
    s00221-014-4053-3; pmid: 25081103

  5. C. Brozzoli, A. C. Roy, L. H. Lidborg, M. Lövdén, Language as a
    tool: Motor proficiency using a tool predicts individual linguistic
    abilities.Front. Psychol. 10 , 1639 (2019). doi:10.3389/
    fpsyg.2019.01639; pmid: 31379674

  6. M. P. Alexander, M. A. Naeser, C. L. Palumbo, Correlations of
    subcortical CT lesion sites and aphasia profiles.Brain 110 ,
    961 – 991 (1987). doi:10.1093/brain/110.4.961; pmid: 3651803

  7. M. Grossmanet al., Grammatical and resource components of
    sentence processing in Parkinson’s disease: An fMRI study.
    Neurology 60 , 775–781 (2003). doi:10.1212/01.
    WNL.0000044398.73241.13; pmid: 12629232

  8. A. Moroet al., Syntax and the brain: Disentangling grammar by
    selective anomalies.Neuroimage 13 , 110–118 (2001).
    doi:10.1006/nimg.2000.0668; pmid: 11133314

  9. M. Teichmannet al., A cortical-subcortical syntax pathway
    linking Broca’s area and the striatum.Hum. Brain Mapp. 36 ,
    2270 – 2283 (2015). doi:10.1002/hbm.22769; pmid: 25682763

  10. M.-L. Brandi, A. Wohlschläger, C. Sorg, J. Hermsdörfer,
    The neural correlates of planning and executing actual tool use.
    J. Neurosci. 34 , 13183–13194 (2014). doi:10.1523/
    JNEUROSCI.0597-14.2014; pmid: 25253863

  11. F. E. Garcea, L. J. Buxbaum, Gesturing tool use and tool
    transport actions modulates inferior parietal functional
    connectivity with the dorsal and ventral object processing
    pathways.Hum. Brain Mapp. 40 , 2867–2883 (2019).
    doi:10.1002/hbm.24565; pmid: 30900321

  12. S. H. Johnson-Frey, R. Newman-Norlund, S. T. Grafton, A
    distributed left hemisphere network active during planning of
    everyday tool use skills.Cereb. Cortex 15 , 681–695 (2005).
    doi:10.1093/cercor/bhh169; pmid: 15342430

  13. S. Obayashiet al., Functional brain mapping of monkey tool
    use.Neuroimage 14 , 853–861 (2001). doi:10.1006/
    nimg.2001.0878; pmid: 11554804

  14. J. Diedrichsen, N. Kriegeskorte, Representational models:
    A common framework for understanding encoding, pattern-
    component, and representational-similarity analysis.
    PLOS Comput. Biol. 13 , e1005508 (2017). doi:10.1371/
    journal.pcbi.1005508; pmid: 28437426

  15. M. V. Peelen, A. J. Wiggett, P. E. Downing, Patterns of fMRI
    activity dissociate overlapping functional brain areas that
    respond to biological motion.Neuron 49 , 815–822 (2006).
    doi:10.1016/j.neuron.2006.02.004; pmid: 16543130

  16. E. Dahlin, A. S. Neely, A. Larsson, L. Bäckman, L. Nyberg,
    Transfer of learning after updating training mediated by the
    striatum.Science 320 , 1510–1512 (2008). doi:10.1126/
    science.1155466; pmid: 18556560

  17. S. M. Jaeggi, M. Buschkuehl, J. Jonides, W. J. Perrig, Improving
    fluid intelligence with training on working memory.Proc. Natl.
    Acad. Sci. U.S.A. 105 , 6829–6833 (2008). doi:10.1073/
    pnas.0801268105; pmid: 18443283

  18. S. M. Jaeggi, M. Buschkuehl, J. Jonides, P. Shah, Short- and
    long-term benefits of cognitive training.Proc. Natl. Acad. Sci.
    U.S.A. 108 , 10081–10086 (2011). doi:10.1073/
    pnas.1103228108; pmid: 21670271

  19. S. Lehéricyet al., Distinct basal ganglia territories are engaged
    in early and advanced motor sequence learning.Proc. Natl.
    Acad. Sci. U.S.A. 102 , 12566–12571 (2005). doi:10.1073/
    pnas.0502762102; pmid: 16107540
    45. H. Makino, E. J. Hwang, N. G. Hedrick, T. Komiyama, Circuit
    mechanisms of sensorimotor learning.Neuron 92 , 705– 721
    (2016). doi:10.1016/j.neuron.2016.10.029; pmid: 27883902
    46. H. H. Yinet al., Dynamic reorganization of striatal circuits
    during the acquisition and consolidation of a skill.Nat.
    Neurosci. 12 , 333–341 (2009). doi:10.1038/nn.2261;
    pmid: 19198605
    47. K. M. Tagarelli, K. F. Shattuck, P. E. Turkeltaub, M. T. Ullman,
    Language learning in the adult brain: A neuroanatomical
    meta-analysis of lexical and grammatical learning.Neuroimage
    193 , 178–200 (2019). doi:10.1016/j.neuroimage.2019.02.061;
    pmid: 30826361
    48. A. M. Graybiel, S. T. Grafton, The striatum: Where skills and
    habits meet.Cold Spring Harb. Perspect. Biol. 7 , a021691
    (2015). doi:10.1101/cshperspect.a021691; pmid: 26238359
    49. K. Amuntset al., Broca’s region: Novel organizational principles
    and multiple receptor mapping.PLOS Biol. 8 , e1000489
    (2010). doi:10.1371/journal.pbio.1000489; pmid: 20877713
    50. G. Papitto, A. D. Friederici, E. Zaccarella, The topographical
    organization of motor processing: An ALE meta-analysis on
    six action domains and the relevance of Broca’s region.
    Neuroimage 206 , 116321 (2020). doi:10.1016/
    j.neuroimage.2019.116321; pmid: 31678500
    51. D. Muretet al., Touch improvement at the hand transfers to
    the face.Curr. Biol. 24 , R736–R737 (2014). doi:10.1016/
    j.cub.2014.07.021; pmid: 25137581
    52. S. Vyaset al., Neural population dynamics underlying motor
    learning transfer.Neuron 97 , 1177–1186.e3 (2018).
    doi:10.1016/j.neuron.2018.01.040; pmid: 29456026
    53. K. Grill-Spector, R. Henson, A. Martin, Repetition and the brain:
    Neural models of stimulus-specific effects.Trends Cogn. Sci.
    10 , 14–23 (2006). doi:10.1016/j.tics.2005.11.006;
    pmid: 16321563
    54. V. Boulengeret al., Cross-talk between language processes
    and overt motor behavior in the first 200 msec of processing.
    J. Cogn. Neurosci. 18 , 1607–1615 (2006). doi:10.1162/
    jocn.2006.18.10.1607; pmid: 17014366
    55. R. N. A. Henson, Neuroimaging studies of priming.
    Prog. Neurobiol. 70 , 53–81 (2003). doi:10.1016/
    S0301-0082(03)00086-8; pmid: 12927334
    56. T. Xuet al., Rapid formation and selective stabilization of
    synapses for enduring motor memories.Nature 462 , 915– 919
    (2009). doi:10.1038/nature08389; pmid: 19946267
    57. E. Wenger, C. Brozzoli, U. Lindenberger, M. Lövdén, Expansion
    and renormalization of human brain structure during skill
    acquisition.Trends Cogn. Sci. 21 , 930–939 (2017).
    doi:10.1016/j.tics.2017.09.008; pmid: 29149999
    58. A. Iriki, M. Taoka, Triadic (ecological, neural, cognitive) niche
    construction: A scenario of human brain evolution
    extrapolating tool use and language from the control of
    reaching actions.Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 ,
    10 – 23 (2012). doi:10.1098/rstb.2011.0190; pmid: 22106423
    59. M. S. Ponce de Leónet al., The primitive brain of earlyHomo.
    Science 372 , 165–171 (2021). doi:10.1126/science.aaz0032;
    pmid: 33833119
    60. D. Stout, T. Chaminade, Stone tools, language and the brain in
    human evolution.Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 ,
    75 – 87 (2012). doi:10.1098/rstb.2011.0099; pmid: 22106428
    61. G. Rizzolatti, M. A. Arbib, Language within our grasp.
    Trends Neurosci. 21 , 188–194 (1998). doi:10.1016/
    s0166-2236(98)01260-0; pmid: 9610880
    62. S. Dehaene, L. Cohen, Cultural recycling of cortical maps.
    Neuron 56 , 384–398 (2007). doi:10.1016/
    j.neuron.2007.10.004; pmid: 17964253
    63. T. J. H. Morganet al., Experimental evidence for the
    co-evolution of hominin tool-making teaching and language.
    Nat. Commun. 6 , 6029 (2015). doi:10.1038/ncomms7029;
    pmid: 25585382
    64. M. L. Anderson, Précis of after phrenology: Neural reuse and
    the interactive brain.Behav. Brain Sci. 39 , e120 (2016).
    pmid: 26077688
    65. W. D. Hopkinset al., Motor skill for tool-use is associated with
    asymmetries in Broca’s area and the motor hand area of
    the precentral gyrus in chimpanzees (Pan troglodytes).Behav.
    Brain Res. 318 , 71–81 (2017). doi:10.1016/j.bbr.2016.10.048;
    pmid: 27816558
    66. P. Lieberman, The evolution of language and thought.
    J. Anthropol. Sci. 94 , 127–146 (2016). pmid: 26963222
    67. R. C. Oldfield, The assessment and analysis of handedness:
    The Edinburgh inventory.Neuropsychologia 9 , 97–113 (1971).
    doi:10.1016/0028-3932(71)90067-4; pmid: 5146491
    68. B. New, C. Pallier, M. Brysbaert, L. Ferrand, Lexique 2: A new
    French lexical database.Behav. Res. Methods Instrum. Comput.
    36 , 516–524 (2004). doi:10.3758/BF03195598;
    pmid: 15641440
    69. J. R. Reynolds, R. West, T. Braver, Distinct neural circuits
    support transient and sustained processes in prospective
    memory and working memory.Cereb. Cortex 19 , 1208– 1221
    (2009). doi:10.1093/cercor/bhn164; pmid: 18854581
    70. L. A. Jones, S. J. Lederman,Human Hand Function
    (Oxford Univ. Press, 2006).
    71. T. Nichols, M. Brett, J. Andersson, T. Wager, J. B. Poline,
    Valid conjunction inference with the minimum statistic.
    Neuroimage 25 , 653–660 (2005). doi:10.1016/
    j.neuroimage.2004.12.005; pmid: 15808966
    72. N. N. Oosterhof, A. C. Connolly, J. V. Haxby, CoSMoMVPA:
    Multi-modal multivariate pattern analysis of neuroimaging data
    in matlab/GNU octave.Front. Neuroinform. 10 , 27 (2016).
    doi:10.3389/fninf.2016.00027; pmid: 27499741
    73. H. Singmann, B. Bolker, J. Westfall, F. Aust, S. M. Ben-Shachar,
    “afex: Analysis of factorial experiments (R Package Version
    0.27-2, 2020);https://CRAN.R-project.org/package=afex.


ACKNOWLEDGMENTS
We thank E. Wenger, A. Farnè, and E. Macaluso for precious advice;
E. Blini for help with parts of the statistical analyses; F. Lamberton
and D. Ibarrola for help with fMRI acquisitions and settings;
F. Leconte for graphic contribution to the figures; F. Volland for
realization of parts of the setup; the research assistants for helping
with the acquisitions; Quercetti for kindly providing the peg-board
games used in the scanner; and S. Alouche, J.-L. Borach, and
C. Farge for administrative support.Funding:C.B. is supported
by Swedish Research Council grants 2015-01717 and Agence
Nationale de le Recherche grant ANR-JC (ANR-16-CE28-0008-01).
M.L. is supported by Swedish Research Council grant 2018-01047.
A.C.R. is supported by ANR-16-CE28-0015. A.C.R. and
V.B. are supported by LabEx ASLAN grants ANR-10-LABX-0081
and ANR-11-IDEX-0007.Author contributions:Conceptualization
and methodology: S.T., M.L., V.B., A.C.R., and C.B. Software,
validation and formal analyses: S.T., R.S., E.K., C.B.; Material
and set-up: S.T., R.S., and E.K.; Investigation and data curation:
S.T., R.P., A.M.G., and C.B.; Original draft preparation and
visualization: S.T., V.B., A.C.R., and C.B.; Writing - review and editing: all
authors.Competing interests:The authors declare no competing
interests.Data and materials availability:Data, materials, and codes
for analyses are available athttps://osf.io/mw3pf/.

SUPPLEMENTARY MATERIALS
science.org/doi/10.1126/science.abe0874
Supplementary Text
Figs. S1 to S4
Tables S1 to S3
References ( 74 , 75 )
Movies S1 and S2
MDAR Reproducibility Checklist

4 August 2020; resubmitted 4 May 2021
Accepted 24 September 2021
10.1126/science.abe0874

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