Volume 17
Number 8
Kitten ganglion cells: dendritic field size at 3
weeks of age and correlation with receptive field size. ANNE C. RUSOFF* AND MARK
W M . DUBIN.
A Colgi study of beta (brisk-X type) ganglion cells has
been done to compare ganglion cells in the retina of
3-week-old and adult cats. An anatomical basis for the
large receptive field centers found in the immature kitten
retina was sought. Kitten beta-type ganglion cells have
significantly smaller dendritic spreads than adult beta
cells; the dendrites of the kitten cells must still grow to
reach their final adult size. Therefore a synoptic basis for
the large receptive field size of the immature cells is suggested.
In 3- and 4-week-old kittens many retinal ganglion cells outside the area centralis have electrophysiologically measured receptive field centers which are larger than those of adult cats.' This
is true whether the receptive field center size is
expressed in degrees of visual angle or converted
to micrometers of retinal extent (to account for the
smaller size of the kitten eye). Although some
fraction of the large center size can be attributed
to cloudy optics in the kitten eye, part of the large
center size reflects neuronal immaturity.1
There are at least three possible anatomical explanations for this neuronal immaturity. (1) The
ganglion cell dendritic field size (which has been
equated with receptive field center size2' 3) may be
larger in kittens than in adults. (2) The center-sign
synapses onto the ganglion cells may be more extensive than those in the adult. (By "center-sign
synapses" we mean those synapses involved in organizing the excitatory, center-type response of
center-surround ganglion cells.) (3) Extensive
center-sign synapses whose effects are normally
masked in the adult cat (by inhibitory activity of
the synapses which comprise the receptive field
surround) may be effective in the kitten. (This
possibility is suggested by the observation that it is
often difficult to elicit responses from the receptive field surround of ganglion cells in kittens.1)
The three explanations are not mutually exclusive.
In all these cases maturation requires removing
part of the anatomical system or masking its effects, that is, 'pruning' of either the dendrites
and/or the synapses. We have tested the idea of
dendritic pruning by measuring the dendritic
fields of Golgi-stained ganglion cells from retinas
of 3-week-old kittens and adult cats. A preliminary
report, which is superceded by this report, has
been presented (ARVO abstract, 1978).
Methods. A modified Golgi-Kopsch-Colonnier
Reports 819
technique (H. Kolb, personal communication) was
used to stain 11 retinas:fiveof adult cats and six of
3-week-old kittens. The retinas were prepared as
flat-mounts with the ganglion cell side up. All
ganglion cells were identified by the presence of
an axon. Identification of ganglion cell type was
made according to the criteria of Boycott and
Wassle.3 All the dendrites of those ganglion cells
which appeared fully stained were drawn at a
magnification of 1000X or 625X with the aid of a
Leitz drawing tube attachment. All cells in which
the dendrites appeared "chopped off" were ignored. The position of each ganglion cell drawn
was noted with respect to the area centralis.
(Blood vessel and optic fiber patterns were used to
determine the position of the area centralis.4) The
longest diameter of each drawing and the diameter
orthogonal to it were measured. The arithmetic
mean of the two diameters was then converted
back into actual length on the retina in micrometers. (The area of each drawing was also measured,
and its geometric mean calculated. Both of these
measurements gave differences in the dendritic
field sizes for the adult and kitten cells equivalent
to those shown in Fig. 2.) Since the amount of
shrinkage which occurred in the Golgi preparations is difficult to know, dendritic field sizes
were not corrected for shrinkage.
Results. Alpha-, beta-, gamma-, and delta-type
ganglion cells were identified in the retinas of both
3-week-old kittens and adult cats. The different
cell types from both kitten and adult retinas appeared qualitatively the same as those described
by Boycott and Wassle3 (Fig. 1).
Fig. 2 is a graph of the dendritic field diameters
of beta cells from both 3-week-old kitten (crosses,
52 cells) and adult cat (diamonds, 42 cells) retinas
plotted vs. distance from the area centralis. Beta
cells were the most commonly found cells which
appeared fully stained; the long dendrites of alpha
and gamma cells often appeared abruptly truncated as if the stain had failed to fill the ends of the
dendrites. Delta cells were seen infrequently.
Therefore insufficient data exist at present to compare the dendritic field sizes of alpha, gamma, and
delta cells between 3-week-old kittens and adult
cats. The beta cell dendritic fields from the adult
cat retinas have approximately the same size range
as those measured by Boycott and Wassle.3 All
adult cells within 2 mm of the area centralis have
dendritic field diameters below 150 /xm, both in
our sample and in that of Boycott and Wassle.
Dendritic field diameter increases with eccentricity; however, no beta cell in either our data or
theirs has a dendritic field diameter greater than
0146-0404/78/0817-0819$00.30/0 © 1978 Assoc. for Res. in Vis. and Ophthal., Inc.
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Invest. Ophthalmol. Visual Sci.
August 1978
820 Reports
V
Fig. 1. Drawing of two beta-type ganglion cells from cat retinas stained by a Golgi technique.
(Beta-type ganglion cells are the anatomical equivalents of brisk-X-type ganglion cells observed in electrophysiological studies.) The cell on the left is from the retina of an adult cat; the
cell is 4.9 mm from the area centralis and has a dendritic field diameter of 177 /xm. The cell on
the right is from the retina of a 3-week-old kitten; the cell is 5.1 mm from the area centralis and
has a dendritic field diameter of 147 fim. The arrows indicate the axon of each cell; the scale
line represents 50 fim.
4UU
• - A d u l t beta
x —Kitten beta
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100
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Distance from area centralis (mm)
Fig. 2. Comparison of the dendritic field diameters of beta-type (brisk-X) ganglion cells from
the retinas of adult cats and from the retinas of 3-week-old kittens. Dendritic field diameter is
plotted vs. retinal eccentricity. Dendritic field diameter is defined here as the arithmetic mean
of the longest diameter of the dendritic field and of the diameter orthogonal to it.
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Volume 17
Number 8
300 (Am. Thus our adult cell measurements agree
very closely with those of Boycott and Wassle.3
However, dendritic field measurements of the
kitten beta cells are very different from the adult
cell measurements. Except in the area centralis
where there are too few adult cells in our sample
for comparison, the 3-week-old kitten cells are
consistently smaller at a given eccentricity on the
retina than are the majority of their adult counterparts. Therefore the dendrites of beta-type ganglion cells in 3-week-old kittens must still grow to
reach their final adult size.
Discussion. Beta cells have been equated with
one of the major physiological classes of cat retinal
ganglion cells—the X cells,3'5 also known as brisk
sustained6 or brisk-X cells.' Therefore, for this one
class of ganglion cells, we can say that the large
receptive field centers measured in 3 (and also
4)-week-old kittens are not caused by dendritic
spreads larger than those of adult cells. It is likely
that either extensive extrasynaptic input of the
center-sign type or the lack of surround-type
synapses onto beta cells is the cause of the large
brisk-X receptive field centers.
We thank Dr. Helga Kolb for providing us with the
procedure for the Golgi technique used here. We also
thank Dr. Richard Mooney for preparing some of the
adult retinas and David Mastronarde for help whenever
needed.
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From the Department of Molecular, Cellular and Developmental Biology, University of Colorado, Boulder.
This work was supported by National Science Foundation Grant BNS76-00506 to M. W. Dubin. Submitted for
publication April 3, 1978. Reprint requests: Mark Wm.
Dubin, MCDB, University of Colorado, Boulder, Colo.
80309. *Present address: Division of Biological Sciences,
University of Michigan, National Science Building, Ann
Arbor, Mich. 48109.
Key words: development, cat, kitten, retina, beta-type
ganglion cells, brisk-X ganglion cells, receptivefieldcenter size
REFERENCES
1. Rusoff, A. C , and Dubin, M. W.: Development of
receptive-field properties of retinal ganglion cells in
kittens, J. Neurophysiol. 40:1188, 1977.
2. Brown, J. E., and Major, D.: Cat retinal ganglion cell
dendritic fields, Exp. Neurol. 15:70, 1966.
3. Boycott, B. B., and Wassle, H.: The morphological
types of ganglion cells of the domestic cat's retina, J.
Physiol. 240:397, 1974.
4. Vakkur, G. J., Bishop, P. O., and Kozak, W.: Visual
optics in the cat, including posterior nodal distance
and retinal landmarks, Vision Res. 3:289, 1963.
5. Levick, W. R.: Form and function of cat retinal ganglion cells, Nature 254:659, 1975.
6. Cleland, B. G., and Levick, W. R.: Brisk and sluggish
concentrically organized ganglion cells in the cat's
retina, J. Physiol. 240:421, 1974.
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