Transneuronal retrograde degeneration of retinal ganglion cells following restricted lesions of striate cortex in the monkey

Abstract. Transneuronal retrograde degeneration of retinal ganglion cells follows extensive striate cortical removal in macaque monkeys. Its extent depends on the age of the monkey at operation, post-operative survival, species and retinal eccentricity. Some studies of human patients with occipital lobe injury have found no evidence for transneuronal retrograde degeneration, suggesting that either degeneration may not occur or, if present, it is caused directly by secondary damage impinging upon the underlying white matter or the blood supply to the dorsal lateral geniculate nucleus and optic tract. We therefore studied retinal ganglion cell degeneration in three macaques in which only the striate cortex corresponding to the macular retina had been removed, thereby sparing extrastriate cortex and precluding interruption of the vascular supply to the thalamus and optic tract. There was extensive loss of ganglion cells in the central retina, corresponding to the central 10° of vision. As the cortical lesion was too small to affect the thalamus or optic tract directly, the retinal degeneration must be transneuronal. Quantitative analysis showed a 65–80% loss of ganglion cells in the corresponding perifoveal retinae along the horizontal meridian. The results confirm that the loss of retinal ganglion cells following striate cortical lesions is predominantly transneuronal.

[1]  J. E. Cason,et al.  A rapid one-step Mallory-Heidenhain stain for connective tissue. , 1950, Stain technology.

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

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

[4]  D. Purves,et al.  Correlated Size Variations in Human Visual Cortex, Lateral Geniculate Nucleus, and Optic Tract , 1997, The Journal of Neuroscience.

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

[6]  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.

[7]  J. Malpeli,et al.  The representation of the visual field in the lateral geniculate nucleus of Macaca mulatta , 1975, The Journal of comparative neurology.

[8]  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.

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

[10]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[11]  S. A. Talbot,et al.  Physiological Studies on Neural Mechanisms of Visual Localization and Discrimination , 1941 .

[12]  W. Skrandies,et al.  Pattern ERGs and VEP topography evoked by lateral eccentric pattern reversal stimulation. , 1988, The International journal of neuroscience.

[13]  G. Kommerell,et al.  [Fundus oculi in homonymous hemianopia]. , 1973, Klinische Monatsblatter fur Augenheilkunde.

[14]  D. Whitteridge,et al.  The representation of the visual field on the cerebral cortex in monkeys , 1961, The Journal of physiology.

[15]  Ettlinger at Bay: can visual agnosia be explained by low-level visual impairments? , 1998 .

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

[17]  A. Cowey,et al.  Retinal ganglion cells labelled from the pulvinar nucleus in macaque monkeys , 1994, Neuroscience.

[18]  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.

[19]  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.

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

[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]  C. B. Shelman,et al.  Morphology of the primate optic nerve. I. Method and total fiber count. , 1972, Investigative ophthalmology.

[23]  Arthur H. Keeney,et al.  The Wholemount Handbook. A Guide to the Preparation and Analysis of Retinal Wholemounts. , 1981 .