Transneuronal retrograde degeneration of retinal ganglion cells and optic tract in hemianopic monkeys and humans.

Transneuronal retrograde degeneration of retinal ganglion cells after removal of primary visual cortex (area V1) is well established by quantitative neurohistological analysis of the ganglion cell layer in monkeys, but remains controversial in human patients. Therefore, we first histologically examined retinal degeneration in sectioned archived retinae of 26 macaque monkeys with unilateral V1 ablation and post-surgical survival times ranging from 3 months to 14.3 years. In addition, the cross-sectional area of the optic tract was measured in archived coronal histological sections of the brain of every hemianopic monkey and in sections from 10 control monkeys with non-visual bilateral cortical lesions. The ratios of nasal and temporal retinal ganglion cell counts in the contralesional eye and ipsi/contralateral optic tract areas were calculated and compared. They show that the decline was initially more pronounced for the optic tract, slackened after 3 years post-lesion and was steeper for the ganglion cells thereafter. Nevertheless, both measures were highly correlated. Second, we calculated ratios from structural magnetic resonance images to see whether the optic tracts of four human hemianopes would show similar evidence of transneuronal degeneration of their ipsilesional optic tract. The results were consistent with extensive and time-dependent degeneration of the retinal ganglion cell layer. The measures of the optic tracts provide evidence for comparable transneuronal retinal ganglion cell degeneration in both primate species and show that structural magnetic resonance image can both reveal and assess it.

[1]  A. Cowey,et al.  Direct and indirect retinal input into degenerated dorsal lateral geniculate nucleus after striate cortical removal in monkey: implications for residual vision , 2004, Experimental Brain Research.

[2]  A. Cowey Atrophy of Retinal Ganglion Cells after Removal of Striate Cortex in a Rhesus Monkey , 1974, Perception.

[3]  F. Riemslag,et al.  Chiasmal misrouting and foveal hypoplasia without albinism , 2006, British Journal of Ophthalmology.

[4]  A. Cowey,et al.  Transneuronal retrograde degeneration of retinal ganglion cells after damage to striate cortex in macaque monkeys: Selective loss of Pβ cells , 1989, Neuroscience.

[5]  H. Bridge,et al.  Imaging reveals optic tract degeneration in hemianopia. , 2011, Investigative ophthalmology & visual science.

[6]  M. Yukie,et al.  Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys , 1981, The Journal of comparative neurology.

[7]  A. Jennekens‐Schinkel Vision, memory and the temporal lobe By Eiichi Iwai and Mortimer Mishkin (eds.), Elsevier, New York, Amsterdam, London, 1990, 453 pages, US$95.00, ISBN 0-444-01531-0 , 1991, Journal of the Neurological Sciences.

[8]  D. Boire,et al.  Transneuronal degeneration of retinal ganglion cells in early hemispherectomized monkeys. , 1999, Neuroreport.

[9]  W. Hoyt,et al.  Optic tract atrophy with cerebral arteriovenous malformations , 1994, Neurology.

[10]  N. Miller,et al.  Transsynaptic degeneration. , 1981, Archives of ophthalmology.

[11]  Wolfgang Reith,et al.  Configuration of the optic chiasm in humans with albinism as revealed by magnetic resonance imaging. , 2003, Investigative ophthalmology & visual science.

[12]  Petra Stoerig,et al.  Blindsight, conscious vision, and the role of primary visual cortex. , 2006, Progress in brain research.

[13]  A. Cowey,et al.  Pattern electroretinograms after cerebral hemispherectomy. , 2001, Brain : a journal of neurology.

[14]  A. Cowey,et al.  The ganglion cell and cone distributions in the monkey's retina: Implications for central magnification factors , 1985, Vision Research.

[15]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[16]  Osman Ratib,et al.  OsiriX: An Open-Source Software for Navigating in Multidimensional DICOM Images , 2004, Journal of Digital Imaging.

[17]  Alan Cowey,et al.  Transneuronal retrograde degeneration of retinal ganglion cells following restricted lesions of striate cortex in the monkey , 2000, Experimental Brain Research.

[18]  J. M. Buren Trans-synaptic retrograde degeneration in the visual system of primates , 1963, Journal of neurology, neurosurgery, and psychiatry.

[19]  A. Cowey,et al.  Blindsight in man and monkey. , 1997, Brain : a journal of neurology.

[20]  Lawrence Weiskrantz,et al.  Hemispheric asymmetry for a visuo-spatial task in monkeys , 1984, Neuropsychologia.

[21]  J. Kaas,et al.  Parameters affecting the loss of ganglion cells of the retina following ablations of striate cortex in primates , 1989, Visual Neuroscience.

[22]  A. Cowey,et al.  Retinal ganglion cells that project to the dorsal lateral geniculate nucleus in the macaque monkey , 1984, Neuroscience.

[23]  A. Cowey,et al.  Variance in transneuronal retrograde ganglion cell degeneration in monkeys after removal of striate cortex: effects of size of the cortical lesion , 1999, Vision Research.

[24]  M. Wong-Riley Changes in the dorsal lateral geniculate nucleus of the squirrel monkey after unilateral ablation of the visual cortex , 1972, The Journal of comparative neurology.

[25]  A. Hendrickson,et al.  Age correlated differences in the amount of retinal degeneration after striate cortex lesions in monkeys. , 1981, Investigative ophthalmology & visual science.

[26]  A. Hendrickson,et al.  Alterations of retinal inputs following striate cortex removal in adult monkey , 2004, Experimental Brain Research.

[27]  B. Wandell,et al.  Topographic Organization of Human Visual Areas in the Absence of Input from Primary Cortex , 1999, The Journal of Neuroscience.

[28]  J. Vonsattel,et al.  Direct demonstration of transsynaptic degeneration in the human visual system: a comparison of retrograde and anterograde changes , 1982, Journal of neurology, neurosurgery, and psychiatry.

[29]  S Zeki,et al.  Conscious visual perception without V1. , 1993, Brain : a journal of neurology.

[30]  Robert W. Kentridge,et al.  Separate processing of texture and form in the ventral stream: evidence from FMRI and visual agnosia. , 2010, Cerebral cortex.

[31]  J. Kulikowski,et al.  Seeing Contour and Colour , 1990, Journal of Cognitive Neuroscience.

[32]  J. Kaas,et al.  Evidence for the loss of X-cells of the retina after long-term ablation of visual cortex in monkeys , 1979, Brain Research.

[33]  B. Falsini,et al.  Retinal ganglion cell dysfunction in humans following post-geniculate lesions: specific spatio–temporal losses revealed by pattern ERG , 1999, Vision Research.

[34]  Saâd Jbabdi,et al.  Changes in connectivity after visual cortical brain damage underlie altered visual function. , 2008, Brain : a journal of neurology.

[35]  A. Cowey,et al.  Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys , 2004, Experimental Brain Research.

[36]  G. Plant,et al.  Retrograde trans-synaptic retinal ganglion cell loss identified by optical coherence tomography. , 2009, Brain : a journal of neurology.

[37]  L. Mihailović,et al.  Changes in the numbers of neurons and glial cells in the lateral geniculate nucleus of the monkey during retrograde cell degeneration , 1971, The Journal of comparative neurology.

[38]  A. Cowey,et al.  Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: implications for residual vision , 2004, Experimental Brain Research.

[39]  V. Buren,et al.  The Retinal Ganglion Cell Layer , 1964 .