Cell and Tissue Research

, Volume 332, Issue 3, pp 461–468 | Cite as

Resolving the three-dimensional myoarchitecture of bovine esophageal wall with diffusion spectrum imaging and tractography

  • Richard J. Gilbert
  • Terry A. Gaige
  • Ruopeng Wang
  • Thomas Benner
  • Guangping Dai
  • Jonathan N. Glickman
  • Van J. Wedeen
Regular Article

Abstract

In order to determine the three-dimensional (3D) resolved muscular anatomy of the mammalian esophagus, we have examined its myoarchitecture with diffusion spectrum magnetic resonance imaging (DSI) and tractography. DSI measures diffusion displacement as a function of magnetic gradients of varied direction and intensity and displays the displacement profile as a 3D contour per voxel. In tractography, the orientation vectors of maximum diffusion/voxel are identified, and intervoxel associations are constructed by a streamline algorithm based on angular similarity in order to generate mesoscale myofiber tracts. We demonstrate that the proximal body of the esophagus consists of helically aligned crossing fiber populations that overlap between layers in the form of a “zipper” region along the length of the tissue. With increasingly distal position along the length of the tissue, helix angle and skeletal muscle prevalence are reduced such that fibers align themselves in the most distal location into distinct inner circular and outer longitudinal smooth muscle layers. We conclude that esophageal myoanatomy consists of crossing myofibers exhibiting a decreasing degree of helicity as a function of axial position and propose that this unique geometric construct provides a mechanism to resist distension and promote aboral flow.

Keywords

Esophageal muscle Myoarchitecture Diffusion weighted magnetic resonance imaging Bovine 

References

  1. Basser PJ (1998) Fiber-tractography via diffusion tensor MRI (DT-MRI). 6th Annual Meeting of the International Society of Magnetic Resonance ISMRM, Sydney, AustraliaGoogle Scholar
  2. Basser PJ, Mattiello J, LeBihan D (1994) MR diffusion tensor spectroscopy and imaging. Biophys J 66:259–267PubMedCrossRefGoogle Scholar
  3. Callaghan PT (1993) Principals of nuclear magnetic resonance microscopy. Clarendon, OxfordGoogle Scholar
  4. Cory DG, Garroway AN (1990) Measurement of translational displacement probabilities by NMR: an indicator of compartmentation. Mag Res Med 14:435–444CrossRefGoogle Scholar
  5. Daivis PJ, Coelho JL (2000) Generalized Fourier law for heat flow in a fluid with a strong, nonuniform strain rate. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 61:6003–6006PubMedGoogle Scholar
  6. Diamant NE (1997) Neuromuscular mechanisms of primary peristalsis. Am J Med 103:40S–43SPubMedCrossRefGoogle Scholar
  7. Fan Y, Gregersen H, Kassab GS (2002) A two-layered mechanical model of the rat esophagus. Experiment and theory. Biomed Eng Online 3:40CrossRefGoogle Scholar
  8. Fung YC (1993) Biomechanics: mechanical properties of living tissues, 2nd edn. Springer, New YorkGoogle Scholar
  9. Gaige TA, Benner T, Wang R, Wedeen VJ, Gilbert RJ (2007) Three dimensional myoarchitecture of the human tongue determined in vivo by high resolution diffusion tensor imaging with tractography. J Magn Reson Imaging 26:654–661PubMedCrossRefGoogle Scholar
  10. Gilbert RJ, Magnusson LH, Napadow VJ, Benner T, Wang R, Wedeen VJ (2006a) Mapping complex myoarchitecture in the bovine tongue with diffusion spectrum magnetic resonance imaging. Biophys J 91:1014–1022PubMedCrossRefGoogle Scholar
  11. Gilbert RJ, Wedeen VJ, Magnusson LH, Benner T, Wang R, Dai G, Napadow VJ, Roche KK (2006b) Three dimensional myoarchitecture of the bovine tongue demonstrated by diffusion spectrum magnetic resonance imaging with tractography. Anatom Rec 288:1173–1182Google Scholar
  12. Kaplunov JD, Wilde MV (2002) Free interfacial vibrations in cylindrical shells. J Acoust Soc Am 111:2692–704PubMedCrossRefGoogle Scholar
  13. Kaplunov JD, Kossovich LY, Wilde MV (2000) Free localized vibrations of a semi-infinite cylindrical shell. J Acoust Soc Am 107:1383–1393PubMedCrossRefGoogle Scholar
  14. Levitsky S, Bergman R, Haddad J (2002) Acoustic waves in cylindrical gap filled by polymeric liquid. Ultrasonics 40:703–706PubMedCrossRefGoogle Scholar
  15. Lin CP, Wedeen VJ, Chen JH, Yao C, Tseng WY (2003) Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms. Neuroimage 19:482–495PubMedCrossRefGoogle Scholar
  16. Nicosia MA, Brasseur JG (2002) A mathematical model of estimating muscle tension in vivo during esophageal bolus transport. J Theor Biol 219:235–255PubMedCrossRefGoogle Scholar
  17. Nicosia MA, Brasseur JG, Liu JB, Miller LS (2001) Local longitudinal muscle shortening of the human esophagus from high-frequency ultrasonography. Am J Physiol Gastrointest Liver Physiol 281:G1022–G1033PubMedGoogle Scholar
  18. Pal A, Brasseur JG (2002) The mechanical advantage of local longitudinal shortening on peristaltic transport. J Biomech Eng 124:94–100PubMedCrossRefGoogle Scholar
  19. Schmahmann JD, Pandya DN, Wang R, Dai G, D’Arceuil HE, de Crespigny AJ, Wedeen VJ (2007) Association of fiber pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 130:630–653PubMedCrossRefGoogle Scholar
  20. Stejskal EO, Tanner JE (1965) Spin diffusion measurements: spin echoes in the presence of a time-dependent field gradient. J Chem Phys 42:288–292CrossRefGoogle Scholar
  21. Takeda T, Kassab G, Liu J, Puckett JL, Mittal RR, Mittal RK (2002) A novel ultrasound technique to study the biomechanics of the human esophagus in vivo. Am J Physiol Gastrointest Liver Physiol 282:G785–G793PubMedGoogle Scholar
  22. Torrey HC (1956) Bloch equations with diffusion terms. Phys Rev 104:563–565CrossRefGoogle Scholar
  23. Tuch DS, Reese TG, Wiegell MR, Makris N, Belliveau JW, Wedeen VJ (2002) High angular resolution diffusion imaging reveals intravoxel white matter fiber heterogeneity. Magn Reson Med 48:577–582PubMedCrossRefGoogle Scholar
  24. Wedeen VJ, Reese TG, Tuch DS, Wiegell MR, Dou J-G, Weisskoff RM, Chessler D (2000) Mapping fiber orientation spectra in cerebral white matter with Fourier-transform diffusion MRI. 8th Annual Meeting of the International Society of Magnetic Resonance Medicine, Denver, ColoradoGoogle Scholar
  25. Yang J, Liao D, Zhao J, Gregersen H (2004) Shear modulus of elasticity of the esophagus. Ann Biomed Eng 32:1223–1230PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Richard J. Gilbert
    • 1
  • Terry A. Gaige
    • 1
  • Ruopeng Wang
    • 2
  • Thomas Benner
    • 2
  • Guangping Dai
    • 2
  • Jonathan N. Glickman
    • 3
  • Van J. Wedeen
    • 2
  1. 1.Department of Mechanical EngineeringMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Athinoula A. Martinos Imaging Center, Department of RadiologyMassachusetts General HospitalBostonUSA
  3. 3.Department of PathologyBrigham and Women’s HospitalBostonUSA

Personalised recommendations