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tion of the dLGN and transneuronal retrograde degenera- to examine the physiological response properties of PMLS
tion of RGCs [4,25,27,40]. The loss of dLGN cells is cortical cells in animals that received a VC lesion and
severe; in adult cats that received a VC lesion on the day of monocular enucleation on the day of birth. Specifically, we
birth, the volume of the dLGN is only 14 of that in recorded PMLS cell responses to visual stimuli in VC-
normal adult cats [15]. Cells that remain have an anomal- lesion animals that had one eye removed at the time of the
ous projection to postero-medial lateral suprasylvian lesion to investigate whether X-like response properties
PMLS extrastriate cortex [7,15,16,24,31]. would develop in PMLS cortex, thereby making PMLS
The degeneration of cells in the retina also is severe cortex more like striate cortex. We hypothesized that
following neonatal VC damage, but it appears to be sparing retinal X-cells after a neonatal VC lesion would
restricted to a single class of RGCs. Following a VC lesion lead to a novel extrastriate X-pathway input along the
on the day of birth, nearly 80 of physiologically iden- enhanced geniculo-PMLS pathway and that this novel
tified retinal X-cells are lost, whereas there is little or no projection would lead to changes in response properties in
loss of Y- or W-cells [27,39,40]. Correspondingly, a loss of PMLS cortical cells that would reflect this novel input,
up to 80 of cells with medium-sized somata has been including higher spatial-frequency tuning, higher spatial
observed following a VC lesion within 1 week of birth resolution, and higher contrast sensitivity compared to
[14,25]. normal PMLS cells.
Physiological studies of extrastriate cortical neurons provide evidence that some functional reorganization
accompanies the changes observed in the retina and dLGN following a neonatal VC lesion [31]. Most cells in normal
2. Materials and methods
adult PMLS cortex are direction selective, respond poorly to flashed stimuli, and can be driven by both eyes. After a
2.1. Subjects VC lesion in adulthood, abnormal response properties are
observed: there is a reduction in the percentage of direc- All procedures used in these experiments were per-
tion-selective cells, an increase in the percentage of cells formed in accordance with NIH guidelines for animal use
that respond to flashed stimuli, and a decrease in the and authorized by protocols approved by the University of
percentage of cells that respond to the ipsilateral eye. This Wisconsin Research Animal Resource Center. Twelve
is true even though there is little or no RGC loss associated animals were used for electrophysiological recording of
with VC damage in adulthood. Despite the large reduction PMLS cortex see Table 1: four normal animals, three
of the dLGN and extensive RGC loss following neonatal animals that received a unilateral VC lesion within 24 h of
VC damage, cells in PMLS develop normal receptive-field birth neonatal lesion, NL, three animals that received a
characteristics [27,39]. This represents a functional com- unilateral VC lesion and monocular enucleation within 24
pensation in that normal response properties develop in h of birth neonatal lesion with enucleation, NL1E, and
PMLS cortex despite the markedly different organization two animals that received a unilateral VC lesion in
of its afferent visual pathways. adulthood and a monocular enucleation on the first day of
A question that arises is why PMLS cells do not take on recording adult lesion with enucleation, AL1E. All
the properties of damaged neurons e.g., in striate cortex animals were born in the laboratory breeding colony, and
following a neonatal VC lesion. One possibility is that animals that received VC lesions survived for at least 6
many properties of striate cortex, such as tuning for high months after VC lesion prior to electrophysiological re-
spatial frequencies and high contrast sensitivity, are sub- cording.
served by the X-pathway [12,13,18,37]. Therefore, perhaps development of striate cortical properties in PMLS cortex
Table 1
following an early VC lesion does not occur because of the
Conditions for each animal used in PMLS recordings
substantial retinal X-cell loss in these animals.
ID Group
Sex Eyes
Lesion Age at
We were interested to find out whether sparing retinal
tested recording
X-cells during a period of anatomical and physiological
96 Normal
F Both
None 4 yrs
plasticity could lead to incorporation of X-like response
139 Normal
F Both
None 5 yrs
properties by PMLS cells. We previously have demon-
4988 Normal
M Both
None 1 yr
4990 Normal
F Both
None 1 yr
strated that monocular enucleation prevents the trans-
K-310 NL
M Both
1 d 2 yrs
neuronal retrograde degeneration of medium-sized RGCs
K-320 NL
F Both
1 d 2 yrs
i.e., X- b-cells following a neonatal VC lesion, possibly
K-339 NL
M Both
1 d 1 yr
by eliminating binocular competition for survival factors in
K-365 NL1E
M Right
1 d 7 months
the dLGN [14]. This RGC sparing might allow X-pathway
K-367 NL1E
F Left
1 d 8 months
K-368 NL1E
M Right
1 d 1 yr
information to be incorporated into remaining cortical
A-49 AL1E
M Right
1 yr 3 yrs
areas, perhaps via the enhanced retino-geniculo-PMLS
A-50 AL1E
F Left
3 yrs 6 yrs
projection. The purpose of the present study was therefore
K .R. Illig et al. Brain Research 882 2000 241 –250
243
2.2. VC lesions 2.4. Visual stimulation
All neonatal and adult lesions were performed under For initial evaluation of neuronal responses, visual
sterile conditions as previously described [28–31,39]. stimuli were presented on the tangent screen with a hand-
Briefly, cats were anaesthetized with 1.5–3.0 halothane held projector. Spots and bars of light were used to
in air, and brain tissue corresponding to areas 17, 18 and determine receptive field location and to map the borders
19 [41] was removed from the left hemisphere by aspira- of the excitatory receptive-field center on the tangent
tion. One eye was removed immediately following the screen. Once the receptive field was mapped, the non-
brain lesion in neonatal-lesion animals, and immediately dominant eye in non-enucleate animals was covered and
prior to recording for adult-lesion animals. All animals the tangent screen was replaced with a display monitor
received a subcutaneous injection of antibiotic solution with a 208 diameter circular aperture, centered on the cell’s
every 48 h for 1 week following the lesion procedure. receptive-field center. Only cells with receptive-fields
smaller than the 208 aperture were included in quantitative 2.3. Recording
tests. Bars and gratings were produced by an Innisfree Image Generator controlled by the computer via a CED
Cats were anesthetized with 4 halothane in air during 1708 Picasso controller.
the initial surgical preparation and maintained with 0.75– Directional selectivity was assessed for each cell to
1.0 halothane in air throughout the experiment. A allow proper configuration of stimuli in subsequent tests.
paralytic solution 1.27 g gallamine triethiodide in 200 ml This was accomplished by moving a sine-wave grating
0.9 saline with 5 dextrose was administered intraven- 78 peak-to-trough contrast; 0.30 cycles degree c d
ously throughout the recording session at a rate that spatial frequency; 3.33 Hz temporal frequency across the
maintained paralysis and provided urinary output typically receptive-field in random order ten times for each of 16
4–8 ml h. The cat was placed in a stereotaxic device different directions 22.58 apart. Blank screens also were
facing a white screen that was 26 cm away and tangent to included as a measure of background firing. The direction
the nodal point of the eyes. The scalp and skull overlying of movement that produced the greatest response was
PMLS cortex were opened to allow placement of the considered the preferred direction for the cell and was used
recording electrode. The pupils were dilated and accom- in all subsequent tests.
modation was blocked pharmacologically. The corneas Once the preferred direction was determined, spatial-
were protected with zero-power contact lenses that in- frequency tuning was assessed by drifting a series of
cluded a 3 mm diameter artificial pupil. Retinal landmarks, sine-wave gratings 78 peak-to-trough contrast of nine
including the area centralis, were reflected and plotted on a different spatial frequencies 0.15–1.35 c d in 0.15 c d
tangent screen using a fiber-optic light source. The eyes increments in random order across the receptive field in
were focused on the tangent screen by sequentially placing the preferred direction. Blank screens also were randomly
spectacle lenses of increasing power in front of the eyes presented for a measure of background activity.
until the fundus projection on the tangent screen was sharp. Following completion of the spatial frequency test, sine-
The position of retinal landmarks was checked periodically wave gratings of the preferred spatial frequency the
throughout the recording session. spatial frequency that elicited the greatest response from
Extracellular single-cell recordings were made with the cell were drifted in the preferred direction at each of
tungsten-in-glass microelectrodes [21] in PMLS cortex seven levels of contrast 1.5, 3, 6, 12, 24, 48, and 78.
ipsilateral to the VC lesion. Despite some shifting of the Again, blank screens were randomly interleaved.
brain and distortion of the hemisphere as a result of the long-term VC lesion, the middle suprasylvian cortex was
2.5. Data analysis easily recognized in all animals by its shape and position
with respect to the ectosylvian gyrus and the posterior For each test, only cells for which a complete set of data
ectosylvian sulcus. Electrode penetrations were made was collected i.e., ten complete trials for every stimulus
down the medial bank of the middle suprasylvian sulcus were included in the analyses. Unit discharges during
roughly parallel to the sulcus within 1–5 mm of the individual stimulus or blank trials were collected in
posterior bend of the sulcus, to correspond to the re- peristimulus time histograms PSTHs with a bin width of
tinotopic location of the cortical lesion and of retinal 10 ms. Responses to grating stimuli were Fourier trans-
degeneration following neonatal VC lesion. Neural activity formed, and the mean61 standard error S.E. of the
was amplified and monitored with an audio monitor and a average neural discharge F0 and the discharge at the
storage oscilloscope. For quantitative analysis, action fundamental frequency of the drifting grating F1 were
potentials were led through a window discriminator to a determined for the ten trials presented in each test. The
computer. Following recording, the electrode was ad- response to the initial cycle of the drifting grating was
vanced at least 100 mm before attempting to record from excluded from the analyses to eliminate the effects of any
another cell. transient response to the stimulus onset. All but three cells
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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
