Deciphering the microstructure of hippocampal subfields with in vivo DTI and NODDI: Applications to experimental multiple sclerosis

Amandine Crombe, Vincent Planche, Gerard Raffard, Julien Bourel, Nadège Dubourdieu, Aude Panatier, Hikaru Fukutomi, Vincent Dousset, Stephane Oliet, Bassem Hiba, Thomas Tourdias
NeuroImage. 2018-05-01; 172: 357-368
DOI: 10.1016/j.neuroimage.2018.01.061

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Crombe A(1), Planche V(2), Raffard G(3), Bourel J(2), Dubourdieu N(2), Panatier A(2), Fukutomi H(4), Dousset V(5), Oliet S(2), Hiba B(6), Tourdias T(7).

Author information:
(1)INSERM, U1215, Neurocentre Magendie, F-33000, Bordeaux, France; Univ. Bordeaux, F-33000, Bordeaux, France; CNRS UMR 5536, Centre de Résonance Magnétique des Systèmes Biologiques, F-33000, Bordeaux, France; CHU de Bordeaux,
F-33000, Bordeaux, France.
(2)INSERM, U1215, Neurocentre Magendie, F-33000, Bordeaux, France; Univ. Bordeaux, F-33000, Bordeaux, France.
(3)Univ. Bordeaux, F-33000, Bordeaux, France; CNRS UMR 5536, Centre de Résonance Magnétique des Systèmes Biologiques, F-33000, Bordeaux, France.
(4)Department of Diagnostic Imaging and Nuclear Medicine, Kyoto University Graduate School of Medicine, Kyoto, Japan.
(5)INSERM, U1215, Neurocentre Magendie, F-33000, Bordeaux, France; Univ. Bordeaux, F-33000, Bordeaux, France; CHU de Bordeaux, F-33000, Bordeaux, France.
(6)Univ. Bordeaux, F-33000, Bordeaux, France; CNRS UMR 5229, Centre de sciences Cognitives, F-69675, Bron, France.
(7)INSERM, U1215, Neurocentre Magendie, F-33000, Bordeaux, France; Univ. Bordeaux, F-33000, Bordeaux, France; CHU de Bordeaux, F-33000, Bordeaux, France.

The hippocampus contains distinct populations of neurons organized into separate
anatomical subfields and layers with differential vulnerability to pathological
mechanisms. The ability of in vivo neuroimaging to pinpoint regional
vulnerability is especially important for better understanding of hippocampal
pathology at the early stage of neurodegenerative disorders and for monitoring
future therapeutic strategies. This is the case for instance in multiple
sclerosis whose neurodegenerative component can affect the hippocampus from the
early stage. We challenged the capacity of two models, i.e. the classical
diffusion tensor imaging (DTI) model and the neurite orientation dispersion and
density imaging (NODDI) model, to compute quantitative diffusion MRI that could
capture microstructural alterations in the individual hippocampal layers of
experimental-autoimmune encephalomyelitis (EAE) mice, the animal model of
multiple sclerosis. To achieve this, the hippocampal anatomy of a healthy mouse
brain was first explored ex vivo with high resolution DTI and NODDI. Then, 18 EAE
mice and 18 control mice were explored 20 days after immunization with in vivo
diffusion MRI prior to sacrifice for the histological quantification of neurites
and glial markers in each hippocampal layer. Fractional anisotropy (FA), axial
diffusivity (AD), radial diffusivity (RD) and mean diffusivity (MD) maps were
computed from the DTI model while the orientation dispersion index (ODI), the
neurite density index (NDI) and the volume fraction of isotropic diffusivity
(isoVF) maps were computed from the NODDI model. We first showed in control mice
that color-coded FA and ODI maps can delineate three main hippocampal layers. The
quantification of FA, AD, RD, MD, ODI, NDI and isoVF presented differences within
these 3 layers, especially within the molecular layer of the dentate gyrus which
displayed a specific signature based on a combination of AD (or MD), ODI and NDI.
Then, the comparison between EAE and control mice showed a decrease of AD
(p = 0.036) and of MD (p = 0.033) selectively within the molecular layer of EAE
mice while NODDI indices did not present any difference between EAE and control
mice in any layer. Histological analyses confirmed the differential vulnerability
of the molecular layer of EAE mice that exhibited decreased dendritic length and
decreased dendritic complexity together with activated microglia. Dendritic
length and intersections within the molecular layer were independent contributors
to the observed decrease of AD (R2 = 0.37 and R2 = 0.40, p


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