Comparison of fiber tracts derived from in-vivo DTI tractography with 3D histological neural tract tracer reconstruction on a macaque brain

Since the introduction of diffusion weighted imaging (DWI) as a method for examining neural connectivity, its accuracy has not been formally evaluated. In this study, we directly compared connections that were visualized using injected neural tract tracers (WGA-HRP) with those obtained using in-vivo diffusion tensor imaging (DTI) tractography. First, we injected the tracer at multiple sites in the brain of a macaque monkey; second, we reconstructed the histological sections of the labeled fiber tracts in 3D; third, we segmented and registered the fibers (somatosensory and motor tracts) with the anatomical in-vivo MRI from the same animal; and last, we conducted fiber tracing along the same pathways on the DTI data using a classical diffusion tracing technique with the injection sites as seeds. To evaluate the performance of DTI fiber tracing, we compared the fibers derived from the DTI tractography with those segmented from the histology. We also studied the influence of the parameters controlling the tractography by comparing Dice superimposition coefficients between histology and DTI segmentations. While there was generally good visual agreement between the two methods, our quantitative comparisons reveal certain limitations of DTI tractography, particularly for regions at remote locations from seeds. We have thus demonstrated the importance of appropriate settings for realistic tractography results.

[1]  Daniel Rueckert,et al.  Nonrigid registration using free-form deformations: application to breast MR images , 1999, IEEE Transactions on Medical Imaging.

[2]  L L Iversen,et al.  The retrograde axonal transport of nerve growth factor. , 1974, Brain research.

[3]  A. Burkhalter,et al.  Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex , 1984, Nature.

[4]  Paul A. Viola,et al.  Alignment by Maximization of Mutual Information , 1997, International Journal of Computer Vision.

[5]  D. Tuch Q‐ball imaging , 2004, Magnetic resonance in medicine.

[6]  H. Kuypers,et al.  Two new fluorescent retrograde neuronal tracers which are transported over long distances , 1980, Neuroscience Letters.

[7]  M. G. Honig,et al.  Fluorescent carbocyanine dyes allow living neurons of identified origin to be studied in long-term cultures , 1986, The Journal of cell biology.

[8]  S. Mori,et al.  Principles of Diffusion Tensor Imaging and Its Applications to Basic Neuroscience Research , 2006, Neuron.

[9]  Susumu Mori,et al.  Magnetic Resonance Diffusion Tensor Microimaging Reveals a Role for Bcl-x in Brain Development and Homeostasis , 2005, The Journal of Neuroscience.

[10]  Vincent Frouin,et al.  Using 3D Non Rigid FFD-Based Method to Register post mortem 3D Histological Data and in vivo MRI of a Baboon Brain , 2003, MICCAI.

[11]  J. Nolte,et al.  The Human Brain , 2013 .

[12]  J. Lavail,et al.  Retrograde Axonal Transport in the Central Nervous System , 1972, Science.

[13]  Carl-Fredrik Westin,et al.  3D Histological Reconstruction of Fiber Tracts and Direct Comparison with Diffusion Tensor MRI Tractography , 2006, MICCAI.

[14]  L. R. Dice Measures of the Amount of Ecologic Association Between Species , 1945 .

[15]  Sears Crowell A Comparison of Shells Utilized by Hydractinia and Podocoryne , 1945 .

[16]  John Nolte,et al.  Human Brain , 1981 .

[17]  M. Solaiyappan,et al.  In vivo three‐dimensional reconstruction of rat brain axonal projections by diffusion tensor imaging , 1999, Magnetic resonance in medicine.

[18]  G. Pearlson,et al.  Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem , 2001, NeuroImage.

[19]  Carl-Fredrik Westin,et al.  Geometrically constrained two-tensor model for crossing tracts in DWI. , 2006, Magnetic resonance imaging.

[20]  M. Mesulam,et al.  Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction product with superior sensitivity for visualizing neural afferents and efferents. , 1978, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[21]  Carl-Fredrik Westin,et al.  Diffusion k-tensor Estimation from Q-ball Imaging Using Discretized Principal Axes , 2006, MICCAI.

[22]  P. Basser,et al.  In vivo fiber tractography using DT‐MRI data , 2000, Magnetic resonance in medicine.

[23]  S. Maier,et al.  Line scan diffusion imaging , 1996, Magnetic resonance in medicine.

[24]  Gudrun Petursdottir,et al.  Fluorescent dextran-amines used as axonal tracers in the nervous system of the chicken embryo , 1986, Journal of Neuroscience Methods.

[25]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[26]  Y. Agid,et al.  Labeled wheat germ agglutinin (WGA) as a new, highly sensitive retrograde tracer in the rat brain hippocampal system , 1978, Brain Research.

[27]  P. Grenier,et al.  MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. , 1986, Radiology.

[28]  P. V. van Zijl,et al.  Three‐dimensional tracking of axonal projections in the brain by magnetic resonance imaging , 1999, Annals of neurology.

[29]  H. Thoenen,et al.  Role of gangliosides in the uptake and retrograde axonal transport of cholera and tetanus toxin as compared to nerve growth factor and wheat germ agglutinin , 1977, Brain Research.

[30]  C. Poupon,et al.  Regularization of Diffusion-Based Direction Maps for the Tracking of Brain White Matter Fascicles , 2000, NeuroImage.

[31]  Ching Yao,et al.  Validation of diffusion spectrum magnetic resonance imaging with manganese-enhanced rat optic tracts and ex vivo phantoms , 2003, NeuroImage.

[32]  Derek K. Jones,et al.  Virtual in Vivo Interactive Dissection of White Matter Fasciculi in the Human Brain , 2002, NeuroImage.

[33]  D. LeBihan,et al.  Validation of q-ball imaging with a diffusion fibre-crossing phantom on a clinical scanner , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[34]  H. Kuypers,et al.  Viruses as transneuronal tracers , 1990, Trends in Neurosciences.

[35]  Carl-Fredrik Westin,et al.  Processing and visualization for diffusion tensor MRI , 2002, Medical Image Anal..

[36]  John Nolte,et al.  The Human Brain An Introduction to Its Functional Anatomy , 2013 .

[37]  N. Logothetis,et al.  Magnetic Resonance Imaging of Neuronal Connections in the Macaque Monkey , 2001, Neuron.

[38]  Ching-Po Lin,et al.  Validation of Diffusion Tensor Magnetic Resonance Axonal Fiber Imaging with Registered Manganese-Enhanced Optic Tracts , 2001, NeuroImage.

[39]  R. Born,et al.  Specificity of Projections from Wide-Field and Local Motion-Processing Regions within the Middle Temporal Visual Area of the Owl Monkey , 2000, The Journal of Neuroscience.