A Jones matrix formalism for simulating three-dimensional polarized light imaging of brain tissue

The neuroimaging technique three-dimensional polarized light imaging (3D-PLI) provides a high-resolution reconstruction of nerve fibres in human post-mortem brains. The orientations of the fibres are derived from birefringence measurements of histological brain sections assuming that the nerve fibres—consisting of an axon and a surrounding myelin sheath—are uniaxial birefringent and that the measured optic axis is oriented in the direction of the nerve fibres (macroscopic model). Although experimental studies support this assumption, the molecular structure of the myelin sheath suggests that the birefringence of a nerve fibre can be described more precisely by multiple optic axes oriented radially around the fibre axis (microscopic model). In this paper, we compare the use of the macroscopic and the microscopic model for simulating 3D-PLI by means of the Jones matrix formalism. The simulations show that the macroscopic model ensures a reliable estimation of the fibre orientations as long as the polarimeter does not resolve structures smaller than the diameter of single fibres. In the case of fibre bundles, polarimeters with even higher resolutions can be used without losing reliability. When taking the myelin density into account, the derived fibre orientations are considerably improved.

[1]  Shalin B. Mehta,et al.  Polarized light microscopy in reproductive and developmental biology , 2015, Molecular reproduction and development.

[2]  Frederike D. Hanke,et al.  Understanding fiber mixture by simulation in 3D Polarized Light Imaging , 2015, NeuroImage.

[3]  Katrin Amunts,et al.  Extracting the inclination angle of nerve fibers within the human brain with 3D-PLI independent of system properties , 2013, Optics & Photonics - Optical Engineering + Applications.

[4]  Veeranna,et al.  Neurofilaments at a glance , 2012, Journal of Cell Science.

[5]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[6]  O. Sporns,et al.  Human connectomics , 2012, Current Opinion in Neurobiology.

[7]  Timo Dickscheid,et al.  High-Resolution Fiber Tract Reconstruction in the Human Brain by Means of Three-Dimensional Polarized Light Imaging , 2011, Front. Neuroinform..

[8]  I. Vitkin,et al.  Tissue polarimetry: concepts, challenges, applications, and outlook. , 2011, Journal of biomedical optics.

[9]  M. Simons,et al.  Central nervous system myelin: structure, synthesis and assembly. , 2011, Trends in cell biology.

[10]  Christoph Palm,et al.  A novel approach to the human connectome: Ultra-high resolution mapping of fiber tracts in the brain , 2011, NeuroImage.

[11]  Peter M. Gayed Neuroscience , 2008, The Yale Journal of Biology and Medicine.

[12]  Lewis D. Griffin,et al.  Polarized light imaging of white matter architecture , 2007, Microscopy research and technique.

[13]  R. Knighton,et al.  Microtubules contribute to the birefringence of the retinal nerve fiber layer. , 2005, Investigative ophthalmology & visual science.

[14]  E. Collett Field Guide to Polarization , 2005 .

[15]  Olaf Sporns,et al.  The Human Connectome: A Structural Description of the Human Brain , 2005, PLoS Comput. Biol..

[16]  Werner Kaminsky,et al.  An automatic optical imaging system for birefringent media , 1996, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[17]  J Beuthan,et al.  The spatial variation of the refractive index in biological cells. , 1996, Physics in medicine and biology.

[18]  H. Persson,et al.  Myelinated nerve fibres in the CNS , 1993, Progress in Neurobiology.

[19]  A. Scheibel,et al.  Fiber composition of the human corpus callosum , 1992, Brain Research.

[20]  R. Martenson Myelin: Biology and Chemistry , 1992 .

[21]  Beardsley Rs The structure of the myelin sheath. Optical studies. , 1971 .

[22]  Blaurock Ae The structure of the myelin sheath: Electron density distribution. Patterson plot. , 1971 .

[23]  R. Jones A New Calculus for the Treatment of Optical Systems. IV. , 1942 .

[24]  R. Jones A New Calculus for the Treatment of Optical SystemsI. Description and Discussion of the Calculus , 1941 .

[25]  R. Jones,et al.  A New Calculus for the Treatment of Optical SystemsII. Proof of Three General Equivalence Theorems , 1941 .

[26]  F. O. Schmitt,et al.  THE ULTRASTRUCTURE OF THE NERVE AXON SHEATH , 1939 .

[27]  R. Bear Optics of nerve myelin , 1936 .

[28]  Olaf Sporns,et al.  The Human Connectome: Linking Structure and Function in the Human Brain , 2009 .

[29]  P. Morell,et al.  Myelin Formation, Structure and Biochemistry , 1999 .

[30]  Max Born Principles of optics - electromagnetic theory of propagation, interference and diffraction of light (7. ed.) , 1999 .

[31]  E D Salmon,et al.  Birefringence of single and bundled microtubules. , 1998, Biophysical journal.

[32]  Francis A. Duck,et al.  Physical properties of tissue : a comprehensive reference book , 1990 .

[33]  H. Lodish Molecular Cell Biology , 1986 .

[34]  B. de Campos Vidal,et al.  Anisotropic properties of the myelin sheath. , 1980, Acta histochemica.

[35]  R. Bear,et al.  The structure of the myelin sheath. Optical studies. , 1971, Neurosciences Research Program bulletin.

[36]  H. Ambronn Das optische Verhalten markhaltiger und markloser Nervenfasern , 1890 .