Selectivity of antibody-mediated destruction of axons in the cat's optic nerve

doi:10.1016/0006-8993(85)90415-9

Brain Research

Volume 336, Issue 1, 10 June 1985, Pages 57-66

https://doi.org/10.1016/0006-8993(85)90415-9 Get rights and content

Abstract

The purpose of this study was to determine the selectivity with which polyspecific antibodies directed against large retinal ganglion cells destroy axons in the cat's optic nerve. Immune serum prepared against large ganglion cells isolated from ox retinas was injected into 1 eye of each of 2 cats. After more than 1 month, the cats were perfused with mixed aldehydes and the optic nerves were prepared for transmission electron microscopy. On the basis of a large sample of micrographs of transverse thin sections, we estimated that each of the nerves that issued from treated eyes contained approximately 62,500 necrotic fibers, amounting to 42–46% of the total fiber population in 1 case and 39–42% in the other. The diameters of 2900–5000 intact axons from each of 4 nerves (2 from immune-treated eyes and 2 from untreated eyes) were measured. Comparisons of histograms of axon diameter for nerves from treated and untreated eyes revealed that 90–100% of large axons with diameters above 3.5–4.0 μm were eliminated by the antibodies. Between 65 and 70% of medium-sized fibers were also eliminated. The number of small axons—those with diameters less than 1.2–1.6 μm — did not differ appreciably from normal. These results suggest that the immune serum destroyed virtually all α cell axons and a substantial fraction of β cell axons but did not reduce the number of small fibers that largely stem from the γ class of retinal ganglion cells.

Reference (49)

AltmanJ. et al.
Selective destruction of the cerebellar cortex with fractionated low-dose X-rays
Exp. Neurol.
(1967)
BallasI. et al.
Retinal projections to the nucleus of the optic tract in the cat as revealed by retrograde transport of horseradish peroxidase
Neurosci. Lett.
(1981)
ChalupaL.M. et al.
Binocular interaction in the fetal cat regulates the size of the ganglion cell population
Neuroscience
(1984)
CookR.D. et al.
The role of oligodendroglia and astroglia in Wallerian degeneration of the optic nerve
Brain Research
(1973)
KornguthS.E. et al.
Antigenic properties of large ganglion cells isolated from ox retina
Exp. Eye Res.
(1981)
KornguthS.E. et al.
Reduction in number of large ganglion cells in cat retina following intravitreous injection of antibodies
Brain Research
(1982)
LennieP.
Parallel visual pathways: a review
Vision Res.
(1980)
BishopG.H. et al.
Further analysis of fibre groups in the optic tract of the cat
Exp. Neurol.
(1969)
BoycottB.B. et al.
The morphological types of ganglion cells of the domestic cat's retina
J. Physiol. (Lond.)
(1974)
ClelandB.G. et al.
Physiological identification of a morphological class of cat retinal ganglion cells
J. Physiol. (Lond.)
(1975)

CrabtreeJ.W. et al.

A dose-response analysis of the effects of antibodies to large ganglion cells on the cat's retinogeniculate pathways

Soc. Neurosci. Abstr.

(1983)

Enroth-CugellC. et al.

The contrast sensitivity of retinal ganglion cells of the cat

J. Physiol. (Lond.)

(1966)

FarmerS.E. et al.

Ganglion cells of the cat accessory optic system: morphology and retinal topography

J. comp. Neurol.

(1982)

FukudaY. et al.

Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina

J. Neurophysiol.

(1974)

GuilleryR.W.

Light and electron-microscopical studies of normal and degenerating axons

HicksS.P. et al.

How to design and build abnormal brains using radiation during development

HughesA.

A quantitative analysis of the cat retinal ganglion cell topography

J. comp. Neurol.

(1975)

IllingR.-B. et al.

The retinal projection of the thalamus in the cat: a quantitative investigation and a comparison with the retinotectal pathway

J. comp. Neurol.

(1981)

JohnsonE.M. et al.

Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor

Science

(1980)

JonssonG.

Chemical neurotoxins as denervation tools in neurobiology

Ann. Rev. Neurosci.

(1980)

KellyJ.P. et al.

The projections of different morphological types of ganglion cells in the cat retina

J. comp. Neurol.

(1975)

KirkD.L. et al.

Axonal conduction latencies of cat retinal ganglion cells in central and peripheral retina

Exp. Brain Res.

(1975)

KolbH. et al.

Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study

Vision Res.

(1982)

LeventhalA.G. et al.

The afferent ganglion cells and cortical projections of the retinal recipient zone of the cat's ‘pulvinar complex’

J. comp. Neurol.

(1980)

Cited by (9)

Effects of antibodies to large retinal ganglion cells on developing retinogeniculate pathways in the cat
1987, Developmental Brain Research
We investigated the effects of polyclonal antibodies, produced against ox large retinal ganglion cells, on the developing retinogeniculate pathways of cats. Four-week-old kittens were given an intraocular injection of either a low or a high concentration of the antibodies and effects were assessed 35–69 weeks later. After a low concentration (110 μg/33 μl volume) injection, the density of retinal α-cells (the morphological counterpart of Y-cells) was reduced 44% in area centralis and 37% in peripheral retina. After a high concentration (333 μg/33 μl volume) injection, α-cell density was reduced 76% in area centralis and 91% in peripheral retina. The same concentration of antibodies had no consistent effect on the numbers of medium- or small-size retinal ganglion cells. Electrophysiological recordings from single neurons in layers A and A₁ of the lateral geniculate nucleus (LGN) revealed a 53% decrease in the percentage of Y-cells after a low-concentration injection and an 82% decrease after a high-concentration injection. There was a concomitant increase in the percentage of LGN cells that were non-responsive to light or that responded too poorly to be classified. No change was observed in the percentages of LGN X-cells or cells with mixed response properties. The reduced encounter rate of LGN Y-cells was not accompanied by significant changes in LGN cell-body size. Together, the results indicate that the immunoablation technique produces a large and apparently selective reduction of the Y-cell retinogeniculate pathway in developing kittens.
Visual field defects in cats with neonatal or adult immunological loss of retinal ganglion cells
1986, Brain Research
Behavioral perimetry methods were used to assess the monocular visual fields of 12 cats that had received intraocular injections of antibodies against large (α/Y) retinal ganglion cells. The antibodies produced defects in head and eye orientation responses to stimuli presented in the nasal visual field of the treated eye; responses to stimuli in the temporal visual hemifield were normal. Similar results were seen in cats that received antibody injections at 4 weeks of age or as adults. In the context of previous results, these findings suggest that a loss of Y cells in the lateral geniculate nucleus is sufficient to reduce geniculocortical function for head and eye orientation to visual stimuli in the nasal visual field.
Integration of Biomarkers Into a Signature Profile of Persistent Traumatic Brain Injury Involving Autoimmune Processes Following Water Hammer Injury From Repetitive Head Impacts
2018, Biomarker Insights
A proposed mechanism for development of CTE following concussive events: Head impact, water hammer injury, neurofilament release, and autoimmune processes
2017, Brain Sciences
Paraneoplastic syndromes
2016, Intraocular Inflammation
Immune-mediated paraneoplasia
2006, British Journal of Biomedical Science

View all citing articles on Scopus

^*: Present address: Section of Neuroanatomy, Yale University School of Medicine, 333 Cedar Street, New Haven, CT 06510, U.S.A.

View full text

Selectivity of antibody-mediated destruction of axons in the cat's optic nerve

Abstract

Exp. Neurol.

Neurosci. Lett.

Neuroscience

Brain Research

Exp. Eye Res.

Brain Research

Vision Res.

Further analysis of fibre groups in the optic tract of the cat

Exp. Neurol.

The morphological types of ganglion cells of the domestic cat's retina

J. Physiol. (Lond.)

Physiological identification of a morphological class of cat retinal ganglion cells

J. Physiol. (Lond.)

A dose-response analysis of the effects of antibodies to large ganglion cells on the cat's retinogeniculate pathways

Soc. Neurosci. Abstr.

The contrast sensitivity of retinal ganglion cells of the cat

J. Physiol. (Lond.)

Ganglion cells of the cat accessory optic system: morphology and retinal topography

J. comp. Neurol.

Retinal distribution and central projections of Y-, X-, and W-cells of the cat's retina

J. Neurophysiol.

Light and electron-microscopical studies of normal and degenerating axons

How to design and build abnormal brains using radiation during development

A quantitative analysis of the cat retinal ganglion cell topography

J. comp. Neurol.

The retinal projection of the thalamus in the cat: a quantitative investigation and a comparison with the retinotectal pathway

J. comp. Neurol.

Dorsal root ganglion neurons are destroyed by exposure in utero to maternal antibody to nerve growth factor

Science

Chemical neurotoxins as denervation tools in neurobiology

Ann. Rev. Neurosci.

The projections of different morphological types of ganglion cells in the cat retina

J. comp. Neurol.

Axonal conduction latencies of cat retinal ganglion cells in central and peripheral retina

Exp. Brain Res.

Amacrine cells, bipolar cells and ganglion cells of the cat retina: a Golgi study

Vision Res.

The afferent ganglion cells and cortical projections of the retinal recipient zone of the cat's ‘pulvinar complex’

J. comp. Neurol.