Skip to main content

Advertisement

SpringerLink
Log in

Connectivity within the primary motor cortex: a DTI tractography study

  • Original Article
  • Published:
Surgical and Radiologic Anatomy Aims and scope Submit manuscript

Abstract

Purpose

Because of the motor function of the precentral area, the connections of the primary motor cortex by white matter fiber bundles have been widely studied in diffusion tensor imaging (DTI). Nevertheless, the connections within the primary motor cortex have yet to be explored. We have studied the connectivity between the different regions of the precentral gyrus in a population of subjects.

Methods

Based on T1 magnetic resonance imaging (MRI) and on individual sulco-gyral anatomy, we defined a parcellation of the right and the left precentral gyri in 20 healthy subjects (10 right-handers; 10 left-handers). This parcellation gave us the opportunity to study MRI tracks reconstructed by tractography within the precentral gyrus and to compare these connections across subjects. We also performed a classical dissection of post-mortem brain tissue to isolate this pattern of connectivity.

Results

We showed MRI tracks connecting the different parts of the same precentral gyrus. This result was reproducible and was found in the left and right hemispheres of the 20 subjects. A quantitative description of the bilateral distribution of the MRI tracks was performed, based on statistical analysis and asymmetry indices, to compare asymmetry and handedness.

Conclusions

To the best of our knowledge, this pattern of connectivity has never before been detailed in the literature. Its functional meaning remains to be determined, which requires further study.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Amunts K, Jancke L, Mohlberg H, Steinmetz H, Zilles K (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender. Neuropsychologia 38:304–312

    Article  CAS  PubMed  Google Scholar 

  2. Amunts K, Schlaug G, Schleicher A, Steinmetz H, Dabringhaus A, Roland PE, Zilles K (1996) Asymmetry in the human motor cortex and handedness. Neuroimage 4:216–222

    Article  CAS  PubMed  Google Scholar 

  3. Annett M (1992) Five tests of hand skill. Cortex 28:583–600

    Article  CAS  PubMed  Google Scholar 

  4. Berman JI, Berger MS, Chung SW, Nagarajan SS, Henry RG (2007) Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg 107:488–494

    Article  PubMed  Google Scholar 

  5. Bernal B, Altman N (2010) The connectivity of the superior longitudinal fasciculus: a tractography DTI study. Magn Reson Imaging 28:217–225

    Article  PubMed  Google Scholar 

  6. Boling W, Olivier A, Bittar RG, Reutens D (1999) Localization of hand motor activation in Broca’s pli de passage moyen. J Neurosurg 91:903–910

    Article  CAS  PubMed  Google Scholar 

  7. Boling W, Olivier A, Fabinyi G (2002) Historical contributions to the modern understanding of function in the central area. Neurosurgery 50:1296–1309 (discussion)

    PubMed  Google Scholar 

  8. Buchel C, Raedler T, Sommer M, Sach M, Weiller C, Koch MA (2004) White matter asymmetry in the human brain: a diffusion tensor MRI study. Cereb Cortex 14:945–951

    Article  CAS  PubMed  Google Scholar 

  9. Catani M, Dell’acqua F, Vergani F, Malik F, Hodge H, Roy P, Valabregue R, de Thiebaut Schotten M (2012) Short frontal lobe connections of the human brain. Cortex 48:273–291

    Article  PubMed  Google Scholar 

  10. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132

    Google Scholar 

  11. Coupe P, Yger P, Prima S, Hellier P, Kervrann C, Barillot C (2008) An optimized blockwise nonlocal means denoising filter for 3-D magnetic resonance images. IEEE Trans Med Imaging 27:425–441

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Dellatolas G, De Agostini M, Jallon P, Poncet M, Rey M, Lellouch J (1988) Mesure de la préférence manuelle par autoquestionnaire dans la population française adulte. Revue de Psychologie aplliquée 38:117–136

    Google Scholar 

  13. Descoteaux M, Deriche R, Knosche TR, Anwander A (2009) Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans Med Imaging 28:269–286

    Article  PubMed  Google Scholar 

  14. Dumas DLR, Oppenheim C, Chassoux F, Rodrigo S, Beuvon F, Daumas-Duport C, Devaux B, Meder JF (2005) Diffusion tensor imaging of partial intractable epilepsy. Eur Radiol 15:279–285

    Article  Google Scholar 

  15. Fillard P, Pennec X, Arsigny V, Ayache N (2007) Clinical DT-MRI estimation, smoothing, and fiber tracking with log-Euclidean metrics. IEEE Trans Med Imaging 26:1472–1482

    Article  PubMed  Google Scholar 

  16. Gerloff C, Bushara K, Sailer A, Wassermann EM, Chen R, Matsuoka T, Waldvogel D, Wittenberg GF, Ishii K, Cohen LG, Hallett M (2006) Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. Brain 129:791–808

    Article  PubMed  Google Scholar 

  17. Geyer S, Ledberg A, Schleicher A, Kinomura S, Schormann T, Burgel U, Klingberg T, Larsson J, Zilles K, Roland PE (1996) Two different areas within the primary motor cortex of man. Nature 382:805–807

    Article  CAS  PubMed  Google Scholar 

  18. Geyer S, Schleicher A, Zilles K (1997) The somatosensory cortex of human: cytoarchitecture and regional distributions of receptor-binding sites. Neuroimage 6:27–45

    Article  CAS  PubMed  Google Scholar 

  19. Gigandet X, Hagmann P, Kurant M, Cammoun L, Meuli R, Thiran JP (2008) Estimating the confidence level of white matter connections obtained with MRI tractography. PLoS One 3:e4006

    Article  PubMed Central  PubMed  Google Scholar 

  20. Gonzalez-Darder JM, Gonzalez-Lopez P, Talamantes F, Quilis V, Cortes V, Garcia-March G, Roldan P (2010) Multimodal navigation in the functional microsurgical resection of intrinsic brain tumors located in eloquent motor areas: role of tractography. Neurosurg Focus 28:E5

    Article  PubMed  Google Scholar 

  21. Guye M, Parker GJ, Symms M, Boulby P, Wheeler-Kingshott CA, Salek-Haddadi A, Barker GJ, Duncan JS (2003) Combined functional MRI and tractography to demonstrate the connectivity of the human primary motor cortex in vivo. Neuroimage 19:1349–1360

    Article  PubMed  Google Scholar 

  22. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008) Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159

    Article  PubMed Central  PubMed  Google Scholar 

  23. Hlustik P, Solodkin A, Gullapalli RP, Noll DC, Small SL (2001) Somatotopy in human primary motor and somatosensory hand representations revisited. Cereb Cortex 11:312–321

    Article  CAS  PubMed  Google Scholar 

  24. Holsapple JW, Preston JB, Strick PL (1991) The origin of thalamic inputs to the “hand” representation in the primary motor cortex. J Neurosci 11:2644–2654

    CAS  PubMed  Google Scholar 

  25. Huang H, Zhang J, Jiang H, Wakana S, Poetscher L, Miller MI, van Zijl PC, Hillis AE, Wytik R, Mori S (2005) DTI tractography based parcellation of white matter: application to the mid-sagittal morphology of corpus callosum. Neuroimage 26:195–205

    Article  PubMed  Google Scholar 

  26. Imfeld A, Oechslin MS, Meyer M, Loenneker T, Jancke L (2009) White matter plasticity in the corticospinal tract of musicians: a diffusion tensor imaging study. Neuroimage 46:600–607

    Article  PubMed  Google Scholar 

  27. Kantelhardt SR, Fadini T, Finke M, Kallenberg K, Siemerkus J, Bockermann V, Matthaeus L, Paulus W, Schweikard A, Rohde V, Giese A (2010) Robot-assisted image-guided transcranial magnetic stimulation for somatotopic mapping of the motor cortex: a clinical pilot study. Acta Neurochir (Wien) 152:333–343

    Article  Google Scholar 

  28. Koch G, Cercignani M, Pecchioli C, Versace V, Oliveri M, Caltagirone C, Rothwell J, Bozzali M (2010) In vivo definition of parieto-motor connections involved in planning of grasping movements. Neuroimage 51:300–312

    Article  PubMed  Google Scholar 

  29. Kumar A, Juhasz C, Asano E, Sundaram SK, Makki MI, Chugani DC, Chugani HT (2009) Diffusion tensor imaging study of the cortical origin and course of the corticospinal tract in healthy children. AJNR Am J Neuroradiol 30:1963–1970

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Lawes IN, Barrick TR, Murugam V, Spierings N, Evans DR, Song M, Clark CA (2008) Atlas-based segmentation of white matter tracts of the human brain using diffusion tensor tractography and comparison with classical dissection. Neuroimage 39:62–79

    Article  PubMed  Google Scholar 

  31. Le Goualher G, Barillot C, Bizais Y (1997) Modeling cortical sulci with active ribbons. IJPRAI 11:1295–1315

    Google Scholar 

  32. Ludwig E, Klingler J (1956) Atlas of human cerebri. Karger, New York

    Google Scholar 

  33. Magro E, Moreau T, Seizeur R, Gibaud B, Morandi X (2012) Characterization of short white matter fiber bundles in the central area from diffusion tensor MRI. Neuroradiology 54:1275–1285

    Article  PubMed  Google Scholar 

  34. Meier JD, Aflalo TN, Kastner S, Graziano MS (2008) Complex organization of human primary motor cortex: a high-resolution fMRI study. J Neurophysiol 100:1800–1812

    Article  PubMed  Google Scholar 

  35. Mori S, van Zijl P (2007) Human white matter atlas. Am J Psychiatry 164:1005

    Article  PubMed  Google Scholar 

  36. Nii Y, Uematsu S, Lesser RP, Gordon B (1996) Does the central sulcus divide motor and sensory functions? Cortical mapping of human hand areas as revealed by electrical stimulation through subdural grid electrodes. Neurology 46:360–367

    Article  CAS  PubMed  Google Scholar 

  37. Oishi K, Zilles K, Amunts K, Faria A, Jiang H, Li X, Akhter K, Hua K, Woods R, Toga AW, Pike GB, Rosa-Neto P, Evans A, Zhang J, Huang H, Miller MI, van Zijl PC, Mazziotta J, Mori S (2008) Human brain white matter atlas: identification and assignment of common anatomical structures in superficial white matter. Neuroimage 43:447–457

    Article  PubMed Central  PubMed  Google Scholar 

  38. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97–113

    Article  CAS  PubMed  Google Scholar 

  39. Ono M, Kubik S, Abernathey C (1990) Atlas of the cerebral sulci. Georg Thieme Verlag, New York

    Google Scholar 

  40. Perrin M, Cointepas Y, Cachia A, Poupon C, Thirion B, Riviere D, Cathier P, El Kouby V, Constantinesco A, Le Bihan D, Mangin JF (2008) Connectivity-Based parcellation of the cortical mantle using q-Ball diffusion imaging. Int J Biomed Imaging 2008:368406

    Article  PubMed Central  PubMed  Google Scholar 

  41. Rathelot JA, Strick PL (2009) Subdivisions of primary motor cortex based on cortico-motoneuronal cells. Proc Natl Acad Sci U S A 106:918–923

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Schaechter JD, Perdue KL, Wang R (2008) Structural damage to the corticospinal tract correlates with bilateral sensorimotor cortex reorganization in stroke patients. Neuroimage 39:1370–1382

    Article  PubMed Central  PubMed  Google Scholar 

  43. Schieber MH (2001) Constraints on somatotopic organization in the primary motor cortex. J Neurophysiol 86:2125–2143

    CAS  PubMed  Google Scholar 

  44. Schmahmann JD, Pandya DN (2007) Cerebral white matter–historical evolution of facts and notions concerning the organization of the fiber pathways of the brain. J Hist Neurosci 16:237–267

    Article  PubMed  Google Scholar 

  45. Thiebaut de Schotten M, Ffytche DH, Bizzi A, Dell’acqua F, Allin M, Walshe M, Murray R, Williams SC, Murphy DG, Catani M (2011) Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography. Neuroimage 54:49–59

    Google Scholar 

  46. Thivard L, Adam C, Hasboun D, Clemenceau S, Dezamis E, Lehericy S, Dormont D, Chiras J, Baulac M, Dupont S (2006) Interictal diffusion MRI in partial epilepsies explored with intracerebral electrodes. Brain 129:375–385

    Article  PubMed  Google Scholar 

  47. Weinstein D, Kindlmann G, Lundberg E (1999) Tensorlines: advection-diffusion based propagation through diffusion tensor fields. IEEE Visualization 249–253

  48. Wiest-Daessle N, Prima S, Morrissey SP, Barillot C (2007) Validation of a new optimisation algorithm for registration yasks in medical imaging. In 4th IEEE International Symposium on Biomedical Imaging 41–44

  49. Wrigley PJ, Gustin SM, Macey PM, Nash PG, Gandevia SC, Macefield VG, Siddall PJ, Henderson LA (2009) Anatomical changes in human motor cortex and motor pathways following complete thoracic spinal cord injury. Cereb Cortex 19:224–232

    Article  CAS  PubMed  Google Scholar 

  50. Yogarajah M, Duncan JS (2008) Diffusion-based magnetic resonance imaging and tractography in epilepsy. Epilepsia 49:189–200

    Article  PubMed  Google Scholar 

  51. Young JP, Geyer S, Grefkes C, Amunts K, Morosan P, Zilles K, Roland PE (2003) Regional cerebral blood flow correlations of somatosensory areas 3a, 3b, 1, and 2 in humans during rest: a PET and cytoarchitectural study. Hum Brain Mapp 19:183–196

    Article  PubMed  Google Scholar 

  52. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120(Pt 1):141–157

    Article  PubMed  Google Scholar 

  53. Zilles K, Amunts K (2010) Centenary of Brodmann’s map–conception and fate. Nat Rev Neurosci 11:139–145

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to warmly thank Alexandre Abadie for his assistance in setting up the data processing chain, Camille Maumet for her assistance in the asymmetry study, Jean-Christophe Gentric for his review of the manuscript and the department of Anatomy of the University of Tours for his assistance in the classical dissection.

Conflict of interest

The authors declare no conflict of interest in the realization of this study.

Author information

Authors and Affiliations

  1. Equipe MediCIS, INSERM U 1099, Faculté de Médecine, University Rennes 1, 35043, Rennes, France

    Tristan Moreau, Bernard Gibaud & Xavier Morandi

  2. Service de Neurochirurgie, CHRU Cavale Blanche, 29200, Brest, France

    Elsa Magro & Romuald Seizeur

  3. Service de Neurochirurgie, CHU Pontchaillou, 35000, Rennes, France

    Xavier Morandi

  4. LaTIM, INSERM UMR 1101, Faculté de Médecine, Université de Bretagne Occidentale, 29200, Brest, France

    Elsa Magro & Romuald Seizeur

  5. Service de Neurochirurgie, Laboratoire d’anatomie, CHU Bretonneau, 37032, Tours, France

    Ilyess Zemmoura

Authors
  1. Elsa Magro
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tristan Moreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Romuald Seizeur
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ilyess Zemmoura
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bernard Gibaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xavier Morandi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elsa Magro.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Magro, E., Moreau, T., Seizeur, R. et al. Connectivity within the primary motor cortex: a DTI tractography study. Surg Radiol Anat 36, 125–135 (2014). https://doi.org/10.1007/s00276-013-1160-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00276-013-1160-y

Keywords

Search

Navigation