In vivo evaluation of optic nerve aging in adult rhesus monkey by diffusion tensor imaging.

Aging of the optic nerve can result in reduced visual sensitivity or vision loss. Normal optic nerve aging has been investigated previously in tissue specimens but poorly explored in vivo. In the present study, the normal aging of optic nerve was evaluated by diffusion tensor imaging (DTI) in non-human primates. Adult female rhesus monkeys at the ages of 9 to 13 years old (young group, n=8) and 21 to 27 years old (old group, n=7) were studied using parallel-imaging-based DTI on a clinical 3T scanner. Compared to young adults, the old monkeys showed 26% lower fractional anisotropy (P<0.01), and 44% greater radial diffusivity, although the latter difference was of marginal statistical significance (P=0.058). These MRI findings are largely consistent with published results of light and electron microscopic studies of optic nerve aging in macaque monkeys, which indicate a loss of fibers and degenerative changes in myelin sheaths.

[1]  Abraham Z. Snyder,et al.  Assessing optic nerve pathology with diffusion MRI: from mouse to human , 2008, NMR in biomedicine.

[2]  B. Pakkenberg,et al.  Marked loss of myelinated nerve fibers in the human brain with age , 2003, The Journal of comparative neurology.

[3]  Heidi Johansen-Berg,et al.  Diffusion MRI at 25: Exploring brain tissue structure and function , 2012, NeuroImage.

[4]  T. Duong,et al.  Effects of common anesthetics on eye movement and electroretinogram , 2011, Documenta Ophthalmologica.

[5]  Hongli Yang,et al.  Physiologic intereye differences in monkey optic nerve head architecture and their relation to changes in early experimental glaucoma. , 2009, Investigative ophthalmology & visual science.

[6]  John Russell,et al.  Dysmyelination Revealed through MRI as Increased Radial (but Unchanged Axial) Diffusion of Water , 2002, NeuroImage.

[7]  John A. Sweeney,et al.  Diffusion Tensor Imaging Study of White Matter Fiber Tracts in Pediatric Bipolar Disorder and Attention-Deficit/Hyperactivity Disorder , 2009, Biological Psychiatry.

[8]  Gareth J. Barker,et al.  Optic nerve diffusion tensor imaging in optic neuritis , 2006, NeuroImage.

[9]  N. Gupta,et al.  Glaucoma as a neurodegenerative disease , 2007, Current opinion in ophthalmology.

[10]  J. Kaas,et al.  The Primate visual system , 2003 .

[11]  Jie Tian,et al.  Quantitative 3-T diffusion tensor imaging in detecting optic nerve degeneration in patients with glaucoma: association with retinal nerve fiber layer thickness and clinical severity , 2013, Neuroradiology.

[12]  Shu-Wei Sun,et al.  Diffusion tensor imaging detects and differentiates axon and myelin degeneration in mouse optic nerve after retinal ischemia , 2003, NeuroImage.

[13]  Gary F. Egan,et al.  Optic nerve diffusion changes and atrophy jointly predict visual dysfunction after optic neuritis , 2009, NeuroImage.

[14]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[15]  G. Dunkelberger,et al.  Aging changes of the rhesus monkey optic nerve. , 1990, Investigative ophthalmology & visual science.

[16]  H. Levkovitch-verbin,et al.  Animal models of optic nerve diseases , 2004, Eye.

[17]  A. Brickman,et al.  White Matter Predictors of Cognitive Functioning in Older Adults , 2012, Journal of the International Neuropsychological Society.

[18]  P. Thompson,et al.  Diffusion imaging, white matter, and psychopathology. , 2011, Annual review of clinical psychology.

[19]  Xiaoping P. Hu,et al.  Enhancing measured diffusion anisotropy in gray matter by eliminating CSF contamination with FLAIR , 2004, Magnetic resonance in medicine.

[20]  J. Sandell,et al.  Effects of age on nerve fibers in the rhesus monkey optic nerve , 2001, The Journal of comparative neurology.

[21]  Sheng-Kwei Song,et al.  Diffusion tensor imaging detected optic nerve injury correlates with decreased compound action potentials after murine retinal ischemia. , 2012, Investigative ophthalmology & visual science.

[22]  R. Harwerth,et al.  Age-related losses of retinal ganglion cells and axons. , 2008, Investigative ophthalmology & visual science.

[23]  C. Lebel,et al.  Diffusion tensor imaging of white matter tract evolution over the lifespan , 2012, NeuroImage.

[24]  P E SYLVESTER,et al.  THE SIZE AND GROWTH OF THE HUMAN OPTIC NERVE , 1961, Journal of neurology, neurosurgery, and psychiatry.

[25]  J. Dubois,et al.  Diffusion tensor imaging of brain development. , 2006, Seminars in fetal & neonatal medicine.

[26]  F. Craik,et al.  Lifelong Bilingualism Maintains White Matter Integrity in Older Adults , 2011, The Journal of Neuroscience.

[27]  C. Sotak,et al.  The role of diffusion tensor imaging in the evaluation of ischemic brain injury – a review , 2002, NMR in biomedicine.

[28]  D. Le Bihan,et al.  Diffusion tensor imaging: Concepts and applications , 2001, Journal of magnetic resonance imaging : JMRI.

[29]  J. H. Howard,et al.  Age‐related differences in multiple measures of white matter integrity: A diffusion tensor imaging study of healthy aging , 2009, Human brain mapping.

[30]  J. Jonas,et al.  Human optic nerve fiber count and optic disc size. , 1992, Investigative ophthalmology & visual science.

[31]  Hangyi Jiang,et al.  Pediatric diffusion tensor imaging: Normal database and observation of the white matter maturation in early childhood , 2006, NeuroImage.

[32]  M R Symms,et al.  In vivo diffusion tensor imaging of the human optic nerve: Pilot study in normal controls , 2006, Magnetic resonance in medicine.

[33]  Christopher G. Filippi,et al.  Magnetic resonance diffusion tensor imaging (MRDTI) and tractography in children with septo-optic dysplasia , 2010, Pediatric Radiology.

[34]  F. Yan,et al.  Time-dependent diffusion tensor changes of optic nerve in patients with indirect traumatic optic neuropathy , 2014, Acta radiologica.

[35]  Axel Sandvig,et al.  Combination of Mn2+‐enhanced and diffusion tensor MR imaging gives complementary information about injury and regeneration in the adult rat optic nerve , 2009, Journal of magnetic resonance imaging : JMRI.

[36]  F. Garaci,et al.  3-T Diffusion tensor imaging of the optic nerve in subjects with glaucoma: correlation with GDx-VCC, HRT-III and Stratus optical coherence tomography findings , 2012, British Journal of Ophthalmology.

[37]  Xiaoping Hu,et al.  In vivo evaluation of optic nerve development in non-human primates by using diffusion tensor imaging , 2014, International Journal of Developmental Neuroscience.

[38]  Alan Peters,et al.  The Effects of Normal Aging on Myelinated Nerve Fibers in Monkey Central Nervous System , 2009, Front. Neuroanat..

[39]  Jun Yoshino,et al.  Demyelination increases radial diffusivity in corpus callosum of mouse brain , 2005, NeuroImage.

[40]  C. Barnes,et al.  Age-related changes in parahippocampal white matter integrity: A diffusion tensor imaging study , 2012, Neuropsychologia.

[41]  J. Morrison,et al.  Age related optic nerve axonal loss in adult Brown Norway rats. , 2005, Experimental eye research.

[42]  D. Friedman,et al.  Primary open-angle glaucoma , 2016, Nature Reviews Disease Primers.

[43]  Linda Chang,et al.  Neuroimaging studies of the aging HIV-1-infected brain , 2012, Journal of NeuroVirology.

[44]  Trevor Andrews,et al.  Magnetic Resonance Diffusion Tensor Imaging of the Optic Nerves to Guide Treatment of Pediatric Suprasellar Tumors , 2009, Pediatric Neurosurgery.

[45]  G. Dunkelberger,et al.  Retinal ganglion cell atrophy correlated with automated perimetry in human eyes with glaucoma. , 1989, American journal of ophthalmology.

[46]  Todd M. Preuss,et al.  Specializations of the Human Visual System: The Monkey Model Meets Human Reality , 2003 .

[47]  J. Sandell,et al.  Effects of age on the glial cells in the rhesus monkey optic nerve , 2002, The Journal of comparative neurology.

[48]  Xiangjun Yang,et al.  Accelerated aging in glaucoma: immunohistochemical assessment of advanced glycation end products in the human retina and optic nerve head. , 2007, Investigative ophthalmology & visual science.

[49]  M. Nicolela,et al.  Rates of neuroretinal rim and peripapillary atrophy area change: a comparative study of glaucoma patients and normal controls. , 2009, Ophthalmology.

[50]  Edward J. Auerbach,et al.  Dose-dependent effect of isoflurane on regional cerebral blood flow in anesthetized macaque monkeys , 2013, Neuroscience Letters.

[51]  E. Wu,et al.  Diffusion Tensor MR Study of Optic Nerve Degeneration in Glaucoma , 2007, 2007 29th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[52]  A. Dale,et al.  Age-related alterations in white matter microstructure measured by diffusion tensor imaging , 2005, Neurobiology of Aging.

[53]  Kathryn Trinkaus,et al.  Optic Nerve Diffusion Tensor Imaging Parameters and Their Correlation With Optic Disc Topography and Disease Severity in Adult Glaucoma Patients and Controls , 2014, Journal of glaucoma.

[54]  Max A. Viergever,et al.  Partial volume effect as a hidden covariate in DTI analyses , 2011, NeuroImage.

[55]  A. Alexander,et al.  Diffusion tensor imaging of the brain , 2007, Neurotherapeutics.

[56]  T. Struffert,et al.  Changes of Radial Diffusivity and Fractional Anisotopy in the Optic Nerve and Optic Radiation of Glaucoma Patients , 2012, TheScientificWorldJournal.

[57]  A. Mccormick,et al.  Aging of the optic nerve. , 1980, Archives of ophthalmology.

[58]  Jian Yang,et al.  In Vivo Evaluation of Retinal and Callosal Projections in Early Postnatal Development and Plasticity Using Manganese-enhanced Mri and Diffusion Tensor Imaging despite the Increasing Number of Studies Investigating Retinotopic and Callosal Projections in Rodent , 2022 .

[59]  Stefan Skare,et al.  How to correct susceptibility distortions in spin-echo echo-planar images: application to diffusion tensor imaging , 2003, NeuroImage.