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tested with grating stimuli responded with an increase in 2.7. Retinal ganglion-cell measurement
both the F0 and F1 components; two cells in AL1E animals and one cell in an NL animal displayed only an F0
Sampling in all animals was restricted to a portion of the response. Otherwise, F0 and F1 responses were highly
hemiretina that undergoes transneuronal retrograde degen- correlated, as described in previous studies [10,11]. Be-
eration in neonatal-lesion animals. Accordingly, 400 mm cause results were similar for the two components, only
square sampling boxes were centered 2.4 mm dorsal to the those obtained for F0 responses are reported.
horizontal meridian and 1.2 mm on either side of the For subsequent analyses of receptive-field size, spatial-
vertical meridian in both hemiretinae, corresponding to frequency tuning, and contrast sensitivity, data were
2108 elevation and 58 azimuth. The visual-field repre- pooled across animals within each group. Justification for
sentation of this region was removed from areas 17, 18 and pooling comes from two observations that strongly suggest
19 in all neonatal-lesion cats as evidenced by the pattern of that responses of individual PMLS cells were independent
degeneration in the dLGN and MIN. Cell measurements of each other. First, these cellular response properties were
were made using methods described previously [14]. independent of cortical position; measures of receptive-
field size, spatial frequency tuning, and contrast sensitivity showed no correlation with electrode position. Second, no
3. Results
clustering of these response properties was observed. Indeed, there were only a few instances where two
3.1. Lesion verification adjacent cells displayed similar results on any one of these
tests, and there were no cases where neighboring cells For all VC-lesion animals NL, NL1E, and AL1E
displayed similar results for all tests. In contrast, the angle groups, the appearance of the cortical surface and the
of preferred line orientation or direction of movement was pattern of retrograde degeneration in the dLGN and MIN
often observed to progress systematically during electrode indicated that area 17 was completely removed. In rare
advancement through the cortex, as reported previously instances, a small representation of the far peripheral visual
[1,45]. field in area 18 was spared. The most common area of
Since all recordings were from the area in the left PMLS cortical sparing was in the representation of the upper
corresponding to the VC lesion, every cell’s receptive field visual field .58 elevation and the far periphery .258
was in the lower contralateral visual field. In the cat, inputs azimuth of area 19 in the inferior portion of the posterior
from the left and right eye each encompass a full repre- suprasylvian gyrus [42]. We attempted to place the record-
sentation of this visual field. Thus, as far as retinal input is ing electrode so that we would sample neurons in PMLS
considered, there should be no difference between animals that had receptive-fields within the retinotopic representa-
with a right- or left-sided enucleation. To confirm this, we tion of damaged cortex for all three areas. However, three
counter-balanced enucleations in each group, and found no PMLS cells had receptive-fields within the retinotopic
overall differences between animals within the enucleated representation of spared cortex for at least one area. The
groups. data for these cells, all of which were from AL1E
animals, were excluded from further analyses. 2.6. Histological preparation and verification of VC
lesion and recording electrode path 3.2. Retinal ganglion-cell measurement
Following each recording session, the animal was Previously, we showed that a monocular enucleation
euthanized with an intravenous injection of a lethal dose of accompanying a VC lesion at 1 week of age prevented
sodium pentobarbital .60 mg kg. Immediately follow- RGC loss in the remaining eye [14]. To determine whether
ing euthanasia, the animal was transcardially perfused with a monocular enucleation also alleviates the RGC loss
4 paraformaldehyde. The eyes were removed and the associated with a cortical lesion received on the day of
retinae were whole-mounted and Nissl-stained [34]. The birth, we compared RGC distributions in the two
brain was removed and immersion-fixed in 4 paraformal- hemiretinae of eyes from each group. Fig. 1 shows the
dehyde for at least 1 h. Coronal sections at 40 mm were results of RGC comparisons for one representative eye
mounted and stained with cresyl violet. The pattern of from each group. Cell sizes are expressed as a percent of
retrograde degeneration in the dLGN and medial interlami- the average of the 10 smallest cells to correct for overall
nar nucleus MIN ipsilateral to the cortical lesion was size differences between nasal and temporal hemiretinae
analyzed to determine the regions of visual-field repre- [14,35]. Each panel represents the difference between the
sentation that were damaged in areas 17, 18 and 19 two hemiretinae in the proportion of cells at each size. An
[29,30]. Surface analyses and examination of serial sec- upward deflection in the curve corresponds to a loss of
tions aided this process. The path of the recording elec- RGCs in the hemiretinae projecting to the damaged
trode through PMLS cortex was confirmed by examining hemisphere for animals with a VC lesion.
serial coronal sections of the brain. When a comparison of RGCs was made between nasal
K .R. Illig et al. Brain Research 882 2000 241 –250
245
there was a severe transneuronal retrograde degeneration of medium-sized RGCs about 180–350 of the size of
2
the smallest cells, or about 120–250 mm in the hemiretina projecting to the damaged hemisphere, Fig.
1B. However, this loss was prevented by monocular enucleation in NL1E animals, and the cell size distribu-
tion in the remaining eye resembled that for normal animals Fig. 1C. These results extend the results of an
earlier study [14], and suggest that retinal X-cells that normally degenerate following a neonatal VC lesion are
spared in NL1E animals. In agreement with previous studies, a VC lesion in adulthood did not produce a loss of
medium-sized RGCs Fig. 1D.
3.3. Visual field sampling and receptive-field size Receptive field centers from 350 neurons were hand-
mapped on the tangent screen Normal n5106; NL n578; NL1E n599; AL1E n567. So that our stimulus would
activate the entire receptive-field center, we only included cells with a center smaller than the size of the display
screen i.e., ,208 diameter in our analyses. Fig. 2 shows a plot of PMLS cell receptive-field center size vs. eccentrici-
ty for these cells. Although the sensitivity of handmapping is not sufficient to yield information about the size or fine
structure of the receptive fields, this plot illustrates that visual-field sampling was similar in all groups. In addition,
no significant differences in receptive-field size among groups were observed ANOVA F
51.90; P.0.10.
3, 346
Thus, sparing medium-sized RGCs after a neonatal VC lesion did not increase the incidence of PMLS cells with
very small, striate-like receptive-field centers.
Fig. 1. Results of RGC comparisons in a representative animal from each group. A Comparison in normal animals, showing very little difference
between the nasal and temporal hemiretinae. B In NL animals, there was a substantial loss of medium-sized RGCs 180–300 of the average
of the size of the 10 smallest RGCs. C By contrast, RGC comparison in NL1E animals revealed no significant lesion-induced loss of RGCs. D
Comparison in AL1E animals indicated no significant loss of RGCs following a lesion in adulthood.
Fig. 2. Receptive-field center size by eccentricity for PMLS cells tested
and temporal hemiretinae in normal animals, a difference
in each group. Note that only cells with receptive-field centers less than
of up to 10 in the proportion of cells of any given size
the size of the stimulus display i.e., ,208 diameter were included in this
was observed Fig. 1A. Following a neonatal VC lesion
study.
246 K
3.4. Spatial-frequency tuning Two measures of spatial-frequency tuning were evalu-
ated in this study. First, the spatial frequency to which each neuron responded with the greatest firing rate was
considered to be the cell’s preferred spatial frequency. We hypothesized that if X-cells were spared in the remaining
eye of NL1E animals, then a greater-than-normal propor- tion of PMLS cells in these animals would display a
preference for higher spatial frequencies. Fig. 3 illustrates two typical spatial-frequency tuning curves observed in the
present study. The distribution of cells in each group Fig. 4A appeared to indicate a shift in preference toward
higher spatial frequencies in the NL1E group. To visual- ize this shift more clearly, the proportion of cells in each
group that exhibited a preferred response to the lowest third 0.15–0.45 c d middle third 0.6–0.9 c d or
highest third 1.05–1.35 c d of the tested spatial fre- quencies is shown in Fig. 4B. Approximately 30 of all
cells in the NL1E group exhibited a preference for the highest spatial frequencies tested 1.05c d, which is
2
significantly greater than in other groups x 543.92, P,
0.001. As a second test of spatial frequency tuning, we
Fig. 4. Spatial frequency responses in each group. A Distribution of cells in each group with the indicated preferred spatial frequency. B
Summary graph depicting the percentage of cells in each group exhibiting a preferred response for the spatial frequencies indicated. P,0.001 with
2
x .
determined each cell’s spatial resolution the highest spatial frequency to which the neuron responded with a
firing rate significantly higher than baseline. As before, a comparison of the distribution of cells in each group Fig.
5A suggested a shift in resolution in the NL1E group toward higher spatial frequency stimuli. The proportion of
Fig. 3. Examples of spatial frequency response curves recorded from PMLS cells. A A cell from a normal animal, illustrating a typical
cells in each group that exhibited low 0.15–0.45 c d,
‘low-pass’ spatial frequency-dependent response, with a preferred spatial
medium 0.6–0.9 c d, or high 1.05 c d spatial
frequency of 0.15 c d and a spatial resolution of 0.45 c d. B A cell
resolution is shown in Fig. 5B. Nearly 40 of cells in the
from a NL1E animal, showing a typical ‘band-pass’ response. This cell
NL1E group responded to the highest frequencies tested
had a preferred spatial frequency of 0.45 c d and a spatial resolution of
1.05 c d which is significantly greater than in any of
0.75 c d. Symbols denote mean response 6S.E. for 10 trials. j5
2
response to sine wave gratings; m5response to blank screen.
the other groups x 562.71, P,0.001.
K .R. Illig et al. Brain Research 882 2000 241 –250
247
Fig. 6. Contrast sensitivity in each group. A Distribution of cells in each group with a significant response at the indicated contrast. B Summary
Fig. 5. Spatial resolution by group. A Distribution of cells in each group graph illustrating the percentage of cells in each group displaying low or
with the indicated spatial resolution. B Summary graph illustrating the
2
high contrast threshold. P,0.001 with x .
percentage of cells in each group exibiting the spatial resolutions
2
indicated. P,0.001 with x .
4. Discussion
