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Cited by 33Hemispheric Asymmetry in NeuroscienceTactile and Sensory InteractionsMotor Control and Adaptation

Development of Right-hemispheric Dominance of Inferior Parietal Lobule in Proprioceptive Illusion Task

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Naito, Eiichi, Morita, Tomoyo, Saito, Daisuke N, Ban, Midori, Shimada, Koji, Okamoto, Yuko, Kosaka, Hirotaka, Okazawa, Hidehiko +1 more·2017·Cerebral Cortex
DOI 10.1093/cercor/bhx223PMC PMC5939204
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Abstract

Functional lateralization can be an indicator of brain maturation. We have consistently shown that, in the adult brain, proprioceptive processing of muscle spindle afferents generating illusory movement of the right hand activates inferior frontoparietal cortical regions in a right-side dominant manner in addition to the cerebrocerebellar motor network. Here we provide novel evidence regarding the development of the right-dominant use of the inferior frontoparietal cortical regions in humans using this task. We studied brain activity using functional magnetic resonance imaging while 60 right-handed blindfolded healthy children (8-11 years), adolescents (12-15 years), and young adults (18-23 years) (20 per group) experienced the illusion. Adult-like right-dominant use of the inferior parietal lobule (IPL) was observed in adolescents, while children used the IPL bilaterally. In contrast, adult-like lateralized cerebrocerebellar motor activation patterns were already observable in children. The right-side dominance progresses during adolescence along with the suppression of the left-sided IPL activity that emerges during childhood. Therefore, the neuronal processing implemented in the adult's right IPL during the proprioceptive illusion task is likely mediated bilaterally during childhood, and then becomes right-lateralized during adolescence at a substantially later time than the lateralized use of the cerebrocerebellar motor system for kinesthetic processing.

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  • Experimentally-induced changes in the perceptual body image (perceived shape and size or posture of the body) have been related to the postcentral sulcus, intraparietal sulcus, insula, and inferior parietal lobule.

    “whereas experimentally‐induced changes in the perceptual body image (perceived shape and size or posture of the body) have been related to the postcentral sulcus, intraparietal sulcus, insula, and inferior parietal lobule (Ehrsson et al., 2005; Kavounoudias et al., 2008; Naito et al., 2017).”

    From Neural bases of the bodily self as revealed by electrical brain stimulation: A systematic review (2023) · cites this paper as Naito et al., 2017

    The Methods describe an experimentally induced illusion of changed hand posture, and the Results and Discussion link illusion-related activity to the inferior parietal lobule and insula. The Results also list areas hIP1 and hIP2, but the retrieved passages do not establish a postcentral-sulcus association or address perceived body shape or size. Thus this paper supports part, but not all, of the collectively cited sentence. (LLM, conf=0.82)

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Research works printed but not linked: 61

  1. Amemiya K, Naito E 2016 Importance of human right inferior frontoparietal network connected by inferior branch of superior longitudinal fasciculus tract in corporeal awareness of kinesthetic illusory movement. Cortex. 78: 15– 30. 26986838
  2. Asato MR, Terwilliger R, Woo J, Luna B 2010 White matter development in adolescence: a DTI study. Cereb Cortex. 20: 2122– 2131. 20051363 PMC2923214
  3. Balsamo LM, Xu B, Grandin CB, Petrella JR, Braniecki SH, Elliott TK, Gaillard WD 2002 A functional magnetic resonance imaging study of left hemisphere language dominance in children. Arch Neurol. 59: 1168– 1174. 12117366
  4. Berlucchi G, Aglioti S 1997 The body in the brain: neural bases of corporeal awareness. Trends Neurosci. 20: 560– 564. 9416668
  5. Biagi L, Cioni G, Fogassi L, Guzzetta A, Sgandurra G, Tosetti M 2016 Action observation network in childhood: a comparative fMRI study with adults. Dev Sci. 19: 1075– 1086. 26537750
  6. Blakemore SJ 2012 Imaging brain development: the adolescent brain. Neuroimage. 61: 397– 406. 22178817
  7. Bosco G, Poppele RE 2001 Proprioception from a spinocerebellar perspective. Physiol Rev. 81: 539– 568. 11274339
  8. Caspers S, Zilles K, Laird AR, Eickhoff SB 2010 ALE meta-analysis of action observation and imitation in the human brain. Neuroimage. 50: 1148– 1167. 20056149 PMC4981639
  9. Catani M, Allin MPG, Husain M, Pugliese L, Mesulam MM, Murray RM, Jones DK 2007 Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci USA. 104: 17163– 17168. 17939998 PMC2040413
  10. Cignetti F, Fontan A, Menant J, Nazarian B, Anton JL, Vaugoyeau M, Assaiante C 2017 Protracted development of the proprioceptive brain network during and beyond adolescence. Cereb Cortex. 27: 1285– 1296. 26733535
  11. Cignetti F, Vaugoyeau M, Nazarian B, Roth M, Anton JL, Assaiante C 2014 Boosted activation of right inferior frontoparietal network: a basis for illusory movement awareness. Hum Brain Mapp. 35: 5166– 5178. 24798824 PMC6869717
  12. Corbetta M, Patel G, Shulman GL 2008 The reorienting system of the human brain: from environment to theory of mind. Neuron. 58: 306– 324. 18466742 PMC2441869
  13. Corbetta M, Shulman GL 2002 Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci. 3: 201– 215. 11994752
  14. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K 2005 A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 25: 1325– 1335. 15850749
  15. Evans AC, Kamber M, Collins DL, MacDonald D 1994 An MRI-based probabilistic atlas of neuroanatomy In: Shorvon SD, editor Magnetic resonance scanning and epilepsy. New York: Plenum Press p. 263– 274.
  16. Everts R, Lidzba K, Wilke M, Kiefer C, Mordasini M, Schroth G, Perrig W, Steinlin M 2009 Strengthening of laterality of verbal and visuospatial functions during childhood and adolescence. Hum Brain Mapp. 30: 473– 483. 18219619 PMC6871185
  17. Fontan A, Cignetti F, Nazarian B, Anton JL, Vaugoyeau M, Assaiante C 2017 How does the body representation system develop in the human brain? Dev Cogn Neurosci. 24: 118– 128. 28314184 PMC6987789
  18. Friston KJ, Holmes AP, Poline JB, Grasby PJ, Williams SC, Frackowiak RS, Turner R 1995 Analysis of fMRI time-series revisited. Neuroimage. 2: 45– 53. 9343589
  19. Goble DJ, Lewis CA, Hurvitz EA, Brown SH 2005 Development of upper limb proprioceptive accuracy in children and adolescents. Hum Mov Sci. 24: 155– 170. 16043248
  20. Goodwin GM, McCloskey DI, Matthews PB 1972 Proprioceptive illusions induced by muscle vibration: contribution by muscle spindles to perception? Science. 175: 1382– 1384. 4258209
  21. 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. 11346886 PMC6871814
  22. Hagura N, Oouchida Y, Aramaki Y, Okada T, Matsumura M, Sadato N, Naito E 2009 Visuokinesthetic perception of hand movement is mediated by cerebro-cerebellar interaction between the left cerebellum and right parietal cortex. Cereb Cortex. 19: 176– 186. 18453537 PMC2638744
  23. Hertz-Pannier L, Chiron C, Jambaque I, Renaux-Kieffer V, Van de Moortele PF, Delalande O, Fohlen M, Brunelle F, Le Bihan D 2002 Late plasticity for language in a child's non-dominant hemisphere. A pre- and post-surgery fMRI study. Brain. 125: 361– 372. 11844736
  24. Hickok G, Poeppel D 2007 The cortical organization of speech processing. Nat Rev Neurosci. 8: 393– 402. 17431404
  25. Holland SK, Plante E, Byars AW, Strawsburg RH, Schmithorst VJ, Ball WS 2001 Normal fMRI brain activation patterns in children performing a verb generation task. Neuroimage. 14: 837– 843. 11554802
  26. Holland SK, Vannest J, Mecoli M, Jacola LM, Tillema JM, Karunanayaka PR, Schmithorst VJ, Yuan W, Plante E, Byars AW 2007 Functional MRI of language lateralization during development in children. Int J Audiol. 46: 533– 551. 17828669 PMC2763431
  27. Holst-Wolf JM, Yeh IL, Konczak J 2016 Development of proprioceptive acuity in typically developing children: normative data on forearm position sense. Front Hum Neurosci. 10: 438 10.3389/fnhum.2016.00436. 27621702 PMC5002403 · DOI
  28. Kang HC, Burgund ED, Lugar HM, Petersen SE, Schlaggara BL 2003 Comparison of functional activation foci in children and adults using a common stereotactic space. Neuroimage. 19: 16– 28. 12781724
  29. Lebel C, Gee M, Camicioli R, Wieler M, Martin W, Beaulieu C 2012 Diffusion tensor imaging of white matter tract evolution over the lifespan. Neuroimage. 60: 340– 352. 22178809
  30. Marini F, Squeri V, Morasso P, Campus C, Konczak J, Masia L 2017 Robot-aided developmental assessment of wrist proprioception in children. J Neuroeng Rehabil. 14: 3 10.1186/s12984-016-0215-9. 28069028 PMC5223571 · DOI
  31. Moro V, Pernigo S, Tsakiris M, Avesani R, Edelstyn NM, Jenkinson PM, Fotopoulou A 2016 Motor versus body awareness: voxel-based lesion analysis in anosognosia for hemiplegia and somatoparaphrenia following right hemisphere stroke. Cortex. 83: 62– 77. 27494375
  32. Morita T, Asada M, Naito E 2016a. Contribution of neuroimaging studies to understanding development of human cognitive brain functions. Front Hum Neurosci. 10: 464 10.3389/fnhum.2016.00464. 27695409 PMC5023663 · DOI
  33. Morita T, Saito DN, Ban M, Shimada K, Okamoto Y, Kosaka H, Okazawa H, Asada M, Naito E 2017 Self-face recognition shares brain regions active during proprioceptive illusion in the right inferior frontoparietal superior longitudinal fasciculus III network. Neuroscience. 348: 288– 301. 28238849
  34. Mountcastle VB, LaMotte RH, Carli G 1972 Detection thresholds for stimuli in humans and monkeys: comparison with threshold events in mechanorecetive afferent nerve fibers innervating monkey hand. J Neurophysiol. 35: 122– 136. 4621505
  35. Nagel BJ, Herting MM, Maxwell EC, Bruno R, Fair D 2013 Hemispheric lateralization of verbal and spatial working memory during adolescence. Brain Cogn. 82: 58– 68. 23511846 PMC3652620
  36. Naito E, Ehrsson HH 2006 Somatic sensation of hand-object interactive movement is associated with activity in the left inferior parietal cortex. J Neurosci. 26: 3783– 3790. 16597731 PMC6674143
  37. Naito E, Ehrsson HH, Geyer S, Zilles K, Roland PE 1999 Illusory arm movements activate cortical motor areas: A positron emission tomography study. J Neurosci. 19: 6134– 6144. 10407049 PMC6783063
  38. Naito E, Matsumoto R, Hagura N, Oouchida Y, Tomimoto H, Hanakawa T 2011 Importance of precentral motor regions in human kinesthesia: a single case study. Neurocase. 17: 133– 147. 20830645
  39. Naito E, Morita T, Amemiya K 2016a. Body representations in the human brain revealed by kinesthetic illusions and their essential contributions to motor control and corporeal awareness. Neurosci Res. 104: 16– 30. 26562333
  40. Naito E, Nakashima T, Kito T, Aramaki Y, Okada T, Sadato N 2007 Human limb-specific and non-limb-specific brain representations during kinesthetic illusory movements of the upper and lower extremities. Eur J Neurosci. 25: 3476– 3487. 17553017
  41. Naito E, Roland PE, Ehrsson HH 2002 I feel my hand moving: a new role of the primary motor cortex in somatic perception of limb movement. Neuron. 36: 979– 988. 12467600
  42. Naito E, Roland PE, Grefkes C, Choi HJ, Eickhoff S, Geyer S, Zilles K, Ehrsson HH 2005 Dominance of the right hemisphere and role of area 2 in human kinesthesia. J Neurophysiol. 93: 1020– 1034. 15385595
  43. Niessen E, Fink GR, Weiss PH 2014 Apraxia, pantomime and the parietal cortex. Neuroimage Clin. 5: 42– 52. 24967158 PMC4066186
  44. Oldfield RC 1971 The assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia. 9: 97– 113. 5146491
  45. Parlatini V, Radua J, Dell'Acqua F, Leslie A, Simmons A, Murphy DG, Catania M, Thiebaut de Schotten M 2017 Functional segregation and integration within frontoparietal networks. Neuroimage. 146: 367– 375. 27639357 PMC5312783
  46. Peeters R, Simone L, Nelissen K, Fabbri-Destro M, Vanduffel W, Rizzolatti G, Orban GA 2009 The representation of tool use in humans and monkeys: common and uniquely human features. J Neurosci. 29: 11523– 11539. 19759300 PMC6665774
  47. Peters BD, Szeszko1 PR, Radua J, Ikuta T, Gruner P, DeRosse P, Zhang JP, Giorgio A, Qiu D, Tapert SF, et al 2012 White matter development in adolescence: diffusion tensor imaging and meta-analytic results. Schizophr Bull. 38: 1308– 1317. 22499780 PMC3494037
  48. Roll JP, Vedel JP 1982 Kinaesthetic role of muscle afferents in man, studied by tendon vibration and microneurography. Exp Brain Res. 47: 177– 190. 6214420
  49. Roll JP, Vedel JP, Ribot E 1989 Alteration of proprioceptive messages induced by tendon vibration in man: a microneurographic study. Exp Brain Res. 76: 213– 222. 2753103
  50. Shmuel A, Augath M, Oeltermann A, Logothetis NK 2006 Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci. 9: 569– 577. 16547508
  51. Shulman GL, Pope DL, Astafiev SV, McAvoy MP, Snyder AZ, Corbetta M 2010 Right hemisphere dominance during spatial selective attention and target detection occurs outside the dorsal frontoparietal network. J Neurosci. 30: 3640– 3651. 20219998 PMC2872555
  52. Smith AT, Williams AL, Singh KD 2004 Negative BOLD in the visual cortex: evidence against blood stealing. Hum Brain Mapp. 21: 213– 220. 15038003 PMC6871689
  53. Springer JA, Binder JR, Hammeke TA, Swanson SJ, Frost JA, Bellgowan PS, Brewer CC, Perry HM, Morris GL, Mueller WM 1999 Language dominance in neurologically normal and epilepsy subjects: a functional MRI study. Brain. 122: 2033– 2045. 10545389
  54. Szaflarski JP, Holland SK, Schmithorst VJ, Byars AW 2006a. An fMRI study of language lateralization in children and adults. Hum Brain Mapp. 27: 202– 212. 16035047 PMC1464420
  55. Szaflarski JP, Schmithorst VJ, Altaye M, Byars AW, Ret J, Plante E, Holland SK 2006b. A longitudinal fMRI study of language development in children age 5–11. Ann Neurol. 59: 796– 807. 16498622 PMC2265796
  56. Szaflarski JP, Rajagopal A, Altaye M, Byars AW, Jacola L, Schmithorst VJ, Schapiro MB, Plante E, Holland SK 2012 Left-handedness and language lateralization in children. Brain Res. 1433C: 85– 97. PMC3249496 22177775
  57. Tiemeier H, Lenroot RK, Greenstein DK, Tran L, Pierson R, Giedd JN 2010 Cerebellum development during childhood and adolescence: a longitudinal morphometric MRI study. Neuroimage. 49: 63– 70. 19683586 PMC2775156
  58. Visser J, Geuze RH 2000 Kinaesthetic acuity in adolescent boys: a longitudinal study. Dev Med Child Neurol. 42: 93– 96. 10698325
  59. Willems RM, Van der Haegen L, Fisher SE, Francks C 2014 On the other hand: including left-handers in cognitive neuroscience and neurogenetics. Nat Rev Neurosci. 15: 193– 201. 24518415
  60. Worsley KJ, Friston KJ 1995 Analysis of fMRI time-series revisited-again. Neuroimage. 2: 173– 181. 9343600
  61. Yuan WH, Szaflarski JP, Schmithorst VJ, Schapiro M, Byars AW, Strawsburg RH, Holland SK 2006 fMRI shows atypical language lateralization in pediatric epilepsy patients. Epilepsia. 47: 593– 600. 16529628 PMC1402337

Cited by

Sorted by citations

Authors
Naito, E., Morita, T., Saito, D. N., Ban, M., Shimada, K., Okamoto, Y., Kosaka, H., Okazawa, H., & Asada, M.
Affiliations
  • Center for Information and Neural Networks (JP)
  • Kanazawa University (JP)
  • Doshisha University (JP)
  • University of Fukui (JP)
Corresponding author
Naito, Eiichi
ORCID
Venue
Cerebral Cortex
Publisher
Oxford University Press (OUP)
Published
2017-08-31
Volume
27
Issue
11
Pages
5385-5397
ISSN
  • 1047-3211 (ISSN-L)
  • 1460-2199
DOI
10.1093/cercor/bhx223
PMC
PMC5939204
OpenAlex
W2752263101
Cited by
33
References
11
Citations by year
2026: 2 · 2025: 1 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 5 · 2020: 3 · 2019: 6 · 2018: 2
FWCI
1.73
Type
journal article
Language
en
Open access
Licence
Locations
  • Cerebral Cortex (publishedVersion, cc-by-nc)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
  • PubMed Central (publishedVersion, cc-by-nc)
  • PubMed (publishedVersion)
Funders
  • Grant-in-Aid for Specially Promoted Research (24000012)
  • Scientific Research on Innovative Areas “Embodied-brain” (JP26120003)
  • Grant-in-Aid for Scientific Research (B) (JP17H02143)
  • Grant-in-Aid for Young Scientists (B) (15K21138)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hemispheric Asymmetry in Neuroscience
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Tactile and Sensory Interactions
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords
proprioception, inferior parietal lobule, right hemisphere dominance, functional lateralization, brain maturation, muscle spindle afferents, children, adolescents, age-related development
MeSH terms
Adolescent, Brain Mapping, Child, Female, Hand, Humans, Illusions, Functional Laterality, Magnetic Resonance Imaging, Male, Movement, Parietal Lobe, Physical Stimulation, Proprioception, Psychophysics, Vibration, Young Adult

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