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Plasticity based on compensatory effector use in the association but not primary sensorimotor cortex of people born without hands.

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Striem-Amit, Ella Vannuscorps, Gilles [UCL] Caramazza, Alfonso

What forces direct brain organization and its plasticity? When brain regions are deprived of their input, which regions reorganize based on compensation for the disability and experience, and which regions show topographically constrained plasticity? People born without hands activate their primary sensorimotor hand region while moving body parts used to compensate for this disability (e.g., their feet). This was taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts, in primary sensorimotor cortex. We tested the selectivity for the compensatory body parts in the primary and association sensorimotor cortex of people born without hands (dysplasic individuals). Despite clear compensatory foot use, the primary sensorimotor hand area in the dysplasic subjects showed preference for adjacent body parts that are not compensatorily used as effectors. This suggests that function-based organization, proposed for congenital blindness and deafness, does not apply to the primary sensorimotor cortex deprivation in dysplasia. These findings stress the roles of neuroanatomical constraints like topographical proximity and connectivity in determining the functional development of primary cortex even in extreme, congenital deprivation. In contrast, increased and selective foot movement preference was found in dysplasics' association cortex in the inferior parietal lobule. This suggests that the typical motor selectivity of this region for manual actions may correspond to high-level action representations that are effector-invariant. These findings reveal limitations to compensatory plasticity and experience in modifying brain organization of early topographical cortex compared with association cortices driven by function-based organization.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2018
Language Anglais
Journal information "Proceedings of the National Academy of Sciences of the United States of America" - Vol. 115, no. 30, p. 7801-7806 (2018)
Peer reviewed yes
Publisher National Academy of Sciences ((United States) Washington, DC)
issn 0027-8424
e-issn 1091-6490
Publication status Publié
Affiliations UCL - SSH/IPSY - Psychological Sciences Research Institute
UCL - SSS/IONS - Institute of NeuroScience
UCL - SSS/IONS/COSY - Systems & cognitive Neuroscience
Keywords Brain development ; Hands ; Motor cortex ; Plasticity ; Somatosensory cortex
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  1. Sanes Jerome N., Donoghue John P., Plasticity and Primary Motor Cortex, 10.1146/annurev.neuro.23.1.393
  2. Makin Tamar R, Cramer Alona O, Scholz Jan, Hahamy Avital, Henderson Slater David, Tracey Irene, Johansen-Berg Heidi, Deprivation-related and use-dependent plasticity go hand in hand, 10.7554/elife.01273
  3. Stoeckel M. C., Seitz R. J., Buetefisch C. M., Congenitally altered motor experience alters somatotopic organization of human primary motor cortex, 10.1073/pnas.0803733106
  4. Hahamy Avital, Macdonald Scott N., van den Heiligenberg Fiona, Kieliba Paullina, Emir Uzay, Malach Rafael, Johansen-Berg Heidi, Brugger Peter, Culham Jody C., Makin Tamar R., Representation of Multiple Body Parts in the Missing-Hand Territory of Congenital One-Handers, 10.1016/j.cub.2017.03.053
  5. Stoeckel M. Cornelia, Jörgens Silke, Witte Otto W., Seitz Rüdiger J., Reduced somatosensory hand representation in thalidomide-induced dysmelia as revealed by fMRI, 10.1111/j.1460-9568.2005.03866.x
  6. Stoeckel M. Cornelia, Pollok Bettina, Witte Otto W., Seitz Rüdiger J., Schnitzler Alfons, Shrinkage of Somatosensory Hand Area in Subjects With Upper Extremity Dysmelia Revealed by Magnetoencephalography, 10.1152/jn.00749.2004
  7. Stoeckel M. C., Pollok B., Schnitzler A., Witte O. W., Seitz R. J., Use-dependent cortical plasticity in thalidomide-induced upper extremity dysplasia: evidence from somaesthesia and neuroimaging, 10.1007/s00221-003-1794-9
  8. Crawford J. Douglas, Henriques Denise Y.P., Medendorp W. Pieter, Three-Dimensional Transformations for Goal-Directed Action, 10.1146/annurev-neuro-061010-113749
  9. Fattori Patrizia, Gamberini Michela, Kutz Dieter F., Galletti Claudio, ‘Arm-reaching’ neurons in the parietal area V6A of the macaque monkey : Arm-reaching neurons in area V6A, 10.1046/j.0953-816x.2001.01618.x
  10. Ferraina S., Johnson P. B., Garasto M. R., Battaglia-Mayer A., Ercolani L., Bianchi L., Lacquaniti F., Caminiti R., Combination of Hand and Gaze Signals During Reaching: Activity in Parietal Area 7m of the Monkey, 10.1152/jn.1997.77.2.1034
  11. Dickinson A. R., Calton J. L., Snyder L. H., Nonspatial Saccade-Specific Activation in area LIP of Monkey Parietal Cortex, 10.1152/jn.00788.2002
  12. Calton Jeffrey L., Dickinson Anthony R., Snyder Lawrence H., Non-spatial, motor-specific activation in posterior parietal cortex, 10.1038/nn862
  13. Hall E.J., Flament D., Fraser C., Lemon R.N., Non-invasive brain stimulation reveals reorganised cortical outputs in amputees, 10.1016/0304-3940(90)90105-i
  14. Kaas, Eur J Phys Rehabil Med, 48, 299 (2012)
  15. Fogassi Leonardo, Luppino Giuseppe, Motor functions of the parietal lobe, 10.1016/j.conb.2005.10.015
  16. Grefkes Christian, Fink Gereon R., REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys : Intraparietal sulcus in monkeys and humans, C. Grefkes and G. R. Fink, 10.1111/j.1469-7580.2005.00426.x
  17. Kaas Jon H., Gharbawie Omar A., Stepniewska Iwona, The Organization and Evolution of Dorsal Stream Multisensory Motor Pathways in Primates, 10.3389/fnana.2011.00034
  18. Vingerhoets Guy, Contribution of the posterior parietal cortex in reaching, grasping, and using objects and tools, 10.3389/fpsyg.2014.00151
  19. Makin Tamar R., Scholz Jan, Henderson Slater David, Johansen-Berg Heidi, Tracey Irene, Reassessing cortical reorganization in the primary sensorimotor cortex following arm amputation, 10.1093/brain/awv161
  20. Lotze M., Phantom movements and pain An fMRI study in upper limb amputees, 10.1093/brain/124.11.2268
  21. MacIver K., Lloyd D. M., Kelly S., Roberts N., Nurmikko T., Phantom limb pain, cortical reorganization and the therapeutic effect of mental imagery, 10.1093/brain/awn124
  22. Foell J., Bekrater-Bodmann R., Diers M., Flor H., Mirror therapy for phantom limb pain: Brain changes and the role of body representation : Mirror therapy for phantom limb pain, 10.1002/j.1532-2149.2013.00433.x
  23. Pons T., Garraghty P., Ommaya A., Kaas J., Taub E, Mishkin M, Massive cortical reorganization after sensory deafferentation in adult macaques, 10.1126/science.1843843
  24. PENFIELD WILDER, BOLDREY EDWIN, SOMATIC MOTOR AND SENSORY REPRESENTATION IN THE CEREBRAL CORTEX OF MAN AS STUDIED BY ELECTRICAL STIMULATION, 10.1093/brain/60.4.389
  25. Geyer Stefan, Schleicher Axel, Zilles Karl, Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex, 10.1006/nimg.1999.0440
  26. Geyer Stefan, Ledberg Anders, Schleicher Axel, Kinomura Shigeo, Schormann Thorsten, Bürgel Uli, Klingberg Torkel, Larsson Jonas, Zilles Karl, Roland Per E., Two different areas within the primary motor cortex of man, 10.1038/382805a0
  27. Zilles Karl, Amunts Katrin, Centenary of Brodmann's map — conception and fate, 10.1038/nrn2776
  28. Amunts K., Schleicher A., Zilles K., Cytoarchitecture of the cerebral cortex—More than localization, 10.1016/j.neuroimage.2007.02.037
  29. 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, San Diego), 2nd Ed, pp 573–602.
  30. Mahon Bradford Z., Caramazza Alfonso, What drives the organization of object knowledge in the brain?, 10.1016/j.tics.2011.01.004
  31. Heimler Benedetta, Striem-Amit Ella, Amedi Amir, Origins of task-specific sensory-independent organization in the visual and auditory brain: neuroscience evidence, open questions and clinical implications, 10.1016/j.conb.2015.09.001
  32. Thaler Lore, Goodale Melvyn A., Echolocation in humans: an overview : Echolocation in humans, 10.1002/wcs.1408
  33. Bi Yanchao, Wang Xiaoying, Caramazza Alfonso, Object Domain and Modality in the Ventral Visual Pathway, 10.1016/j.tics.2016.02.002
  34. Ricciardi Emiliano, Handjaras Giacomo, Pietrini Pietro, The blind brain: How (lack of) vision shapes the morphological and functional architecture of the human brain, 10.1177/1535370214538740
  35. Merzenich M.M., Kaas J.H., Wall J., Nelson R.J., Sur M., Felleman D., Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation, 10.1016/0306-4522(83)90024-6
  36. Bock Andrew S., Fine Ione, Anatomical and functional plasticity in early blind individuals and the mixture of experts architecture, 10.3389/fnhum.2014.00971
  37. Renier Laurent, De Volder Anne G., Rauschecker Josef P., Cortical plasticity and preserved function in early blindness, 10.1016/j.neubiorev.2013.01.025
  38. Ptito Maurice, Matteau Isabelle, Gjedde Albert, Kupers Ron, Recruitment of the middle temporal area by tactile motion in congenital blindness : , 10.1097/wnr.0b013e3283279909
  39. Lomber Stephen G., What is the function of auditory cortex when it develops in the absence of acoustic input?, 10.1016/j.cogdev.2017.02.007
  40. Bola Łukasz, Zimmermann Maria, Mostowski Piotr, Jednoróg Katarzyna, Marchewka Artur, Rutkowski Paweł, Szwed Marcin, Task-specific reorganization of the auditory cortex in deaf humans, 10.1073/pnas.1609000114
  41. Striem-Amit Ella, Vannuscorps Gilles, Caramazza Alfonso, Sensorimotor-independent development of hands and tools selectivity in the visual cortex, 10.1073/pnas.1620289114
  42. Bedny Marina, Evidence from Blindness for a Cognitively Pluripotent Cortex, 10.1016/j.tics.2017.06.003
  43. Amedi Amir, Hofstetter Shir, Maidenbaum Shachar, Heimler Benedetta, Task Selectivity as a Comprehensive Principle for Brain Organization, 10.1016/j.tics.2017.03.007
  44. Campus Claudio, Sandini Giulio, Concetta Morrone Maria, Gori Monica, Spatial localization of sound elicits early responses from occipital visual cortex in humans, 10.1038/s41598-017-09142-z
  45. Kaas J H, Merzenich M M, Killackey H P, The Reorganization of Somatosensory Cortex Following Peripheral Nerve Damage in Adult and Developing Mammals, 10.1146/annurev.ne.06.030183.001545
  46. Striem-Amit Ella, Almeida Jorge, Belledonne Mario, Chen Quanjing, Fang Yuxing, Han Zaizhu, Caramazza Alfonso, Bi Yanchao, Topographical functional connectivity patterns exist in the congenitally, prelingually deaf, 10.1038/srep29375
  47. Striem-Amit Ella, Ovadia-Caro Smadar, Caramazza Alfonso, Margulies Daniel S., Villringer Arno, Amedi Amir, Functional connectivity of visual cortex in the blind follows retinotopic organization principles, 10.1093/brain/awv083
  48. Bock A. S., Binda P., Benson N. C., Bridge H., Watkins K. E., Fine I., Resting-State Retinotopic Organization in the Absence of Retinal Input and Visual Experience, 10.1523/jneurosci.4715-14.2015
  49. Schieber Marc H., Constraints on Somatotopic Organization in the Primary Motor Cortex, 10.1152/jn.2001.86.5.2125
  50. Ramachandran V., Rogers-Ramachandran D, Stewart M, Perceptual correlates of massive cortical reorganization, 10.1126/science.1439826
  51. Rauschecker Josef P., Auditory cortical plasticity: a comparison with other sensory systems, 10.1016/s0166-2236(98)01303-4
  52. Kaas J., Krubitzer L., Chino Y., Langston A., Polley E., Blair N, Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina, 10.1126/science.2326637
  53. Kami Avi, Meyer Gundela, Jezzard Peter, Adams Michelle M., Turner Robert, Ungerleider Leslie G., Functional MRI evidence for adult motor cortex plasticity during motor skill learning, 10.1038/377155a0
  54. Nudo RJ, Milliken GW, Jenkins WM, Merzenich MM, Use-dependent alterations of movement representations in primary motor cortex of adult squirrel monkeys, 10.1523/jneurosci.16-02-00785.1996
  55. Janssen Peter, Scherberger Hansjörg, Visual Guidance in Control of Grasping, 10.1146/annurev-neuro-071714-034028
  56. Jain N., Qi H.-X., Collins C. E., Kaas J. H., Large-Scale Reorganization in the Somatosensory Cortex and Thalamus after Sensory Loss in Macaque Monkeys, 10.1523/jneurosci.2334-08.2008
  57. Martel Marie, Cardinali Lucilla, Roy Alice C., Farnè Alessandro, Tool-use: An open window into body representation and its plasticity, 10.1080/02643294.2016.1167678
  58. Goldenberg G., Spatt J., The neural basis of tool use, 10.1093/brain/awp080
  59. Tarhan Leyla Y., Watson Christine E., Buxbaum Laurel J., Shared and Distinct Neuroanatomic Regions Critical for Tool-related Action Production and Recognition: Evidence from 131 Left-hemisphere Stroke Patients, 10.1162/jocn_a_00876
  60. Caspers Svenja, Zilles Karl, Laird Angela R., Eickhoff Simon B., ALE meta-analysis of action observation and imitation in the human brain, 10.1016/j.neuroimage.2009.12.112
  61. Tunik E., Rice N.J., Hamilton A., Grafton S.T., Beyond grasping: Representation of action in human anterior intraparietal sulcus, 10.1016/j.neuroimage.2007.03.026
  62. Leshinskaya Anna, Caramazza Alfonso, Abstract categories of functions in anterior parietal lobe, 10.1016/j.neuropsychologia.2015.01.014
  63. Gallivan J. P., McLean D. A., Flanagan J. R., Culham J. C., Where One Hand Meets the Other: Limb-Specific and Action-Dependent Movement Plans Decoded from Preparatory Signals in Single Human Frontoparietal Brain Areas, 10.1523/jneurosci.0541-12.2013
  64. Gallivan J. P., McLean D. A., Smith F. W., Culham J. C., Decoding Effector-Dependent and Effector-Independent Movement Intentions from Human Parieto-Frontal Brain Activity, 10.1523/jneurosci.1058-11.2011
  65. Haar Shlomi, Dinstein Ilan, Shelef Ilan, Donchin Opher, Effector-Invariant Movement Encoding in the Human Motor System, 10.1523/jneurosci.1663-17.2017
  66. Ogawa Kenji, Imai Fumihito, Hand-independent representation of tool-use pantomimes in the left anterior intraparietal cortex, 10.1007/s00221-016-4765-7
  67. H. SCHIEBER MARC, K. DEUEL RUTHMARY, Primary motor cortex reorganization in a long-term monkey amputee, 10.1080/08990229771024
  68. Heed Tobias, Leone Frank T. M., Toni Ivan, Medendorp W. Pieter, Functional versus effector-specific organization of the human posterior parietal cortex: revisited, 10.1152/jn.00312.2014
  69. Jacobs Stéphane, Danielmeier Claudia, Frey Scott H., Human Anterior Intraparietal and Ventral Premotor Cortices Support Representations of Grasping with the Hand or a Novel Tool, 10.1162/jocn.2009.21372
  70. Lewis James W., Cortical Networks Related to Human Use of Tools, 10.1177/1073858406288327
  71. Gallivan J. P., Cavina-Pratesi C., Culham J. C., Is That within Reach? fMRI Reveals That the Human Superior Parieto-Occipital Cortex Encodes Objects Reachable by the Hand, 10.1523/jneurosci.0377-09.2009
  72. Peeters R., Simone L., Nelissen K., Fabbri-Destro M., Vanduffel W., Rizzolatti G., Orban G. A., The Representation of Tool Use in Humans and Monkeys: Common and Uniquely Human Features, 10.1523/jneurosci.2040-09.2009
  73. Talairach J Tournoux P (1988) Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York).
  74. Friston K. J., Worsley K. J., Frackowiak R. S. J., Mazziotta J. C., Evans A. C., Assessing the significance of focal activations using their spatial extent : Assessing Focal Activations by Spatial Extent, 10.1002/hbm.460010306
  75. Friston Karl J., Holmes Andrew P., Worsley Keith J., How Many Subjects Constitute a Study?, 10.1006/nimg.1999.0439
  76. Eickhoff Simon B., Stephan Klaas E., Mohlberg Hartmut, Grefkes Christian, Fink Gereon R., Amunts Katrin, Zilles Karl, A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data, 10.1016/j.neuroimage.2004.12.034
  77. Jeffreys H (1998) The Theory of Probability (Oxford Univ Press, Oxford).
  78. Flor H., Elbert T., Knecht S., Wienbruch C., Pantev C., Birbaumers N., Larbig W., Taub E., Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation, 10.1038/375482a0
  79. Rouder Jeffrey N., Speckman Paul L., Sun Dongchu, Morey Richard D., Iverson Geoffrey, Bayesian t tests for accepting and rejecting the null hypothesis, 10.3758/pbr.16.2.225
  80. Biswal Bharat, Zerrin Yetkin F., Haughton Victor M., Hyde James S., Functional connectivity in the motor cortex of resting human brain using echo-planar mri, 10.1002/mrm.1910340409
  81. Glasser Matthew F., Coalson Timothy S., Robinson Emma C., Hacker Carl D., Harwell John, Yacoub Essa, Ugurbil Kamil, Andersson Jesper, Beckmann Christian F., Jenkinson Mark, Smith Stephen M., Van Essen David C., A multi-modal parcellation of human cerebral cortex, 10.1038/nature18933
  82. Meier Jeffrey D., Aflalo Tyson N., Kastner Sabine, Graziano Michael S. A., Complex Organization of Human Primary Motor Cortex: A High-Resolution fMRI Study, 10.1152/jn.90531.2008
  83. Strother Lars, Medendorp W. Pieter, Coros Alexandra M., Vilis Tutis, Double representation of the wrist and elbow in human motor cortex : Double representation of the wrist and elbow, 10.1111/j.1460-9568.2012.08241.x
  84. Philip B. A., Frey S. H., Compensatory Changes Accompanying Chronic Forced Use of the Nondominant Hand by Unilateral Amputees, 10.1523/jneurosci.3770-13.2014
Bibliographic reference Striem-Amit, Ella ; Vannuscorps, Gilles ; Caramazza, Alfonso. Plasticity based on compensatory effector use in the association but not primary sensorimotor cortex of people born without hands.. In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 115, no. 30, p. 7801-7806 (2018)
Permanent URL http://hdl.handle.net/2078.1/203195