Age-Dependent Sparing of Visual Function After Bilateral Lesions of

Primary Visual Cortex

R. Jarrett Rushmore, Laura Rigolo,
Amanda K. Peer, and Linda M. Afifi
Boston University School of Medicine
Antoni Valero-Cabre
Boston University School of Medicine
and Fondation Ophtalmologique Rothschild
Bertram R. Payne
Boston University School of Medicine
Bilateral lesions of primary visual cortex (PVC) sustained early in life induce the visual system to
undergo structural and functional reorganization and produce modified neuronal networks capable of
mediating visual abilities that would be impaired if the lesions occurred in adulthood. Reorganization
after early lesion is also accompanied by degeneration of the lateral geniculate nucleus of the thalamus,
and 90% of beta retinal ganglion cells die via retrograde degeneration. It is unclear whether the high
potential of the system to reorganize after early lesion could overcome the effects of beta retinal ganglion
cell death. Visual acuity, which depends on an intact beta-cell array, was impaired in cats that underwent
PVC lesions on postnatal day 1 and indicated that neuroplastic potential was insufficient to overcome
early lesion-induced maladaptive plasticity. Animals with lesions made at 1 month of age, a stage
accompanied by high levels of neuroplastic potential but no death of beta cells, achieved acuity measures
equivalent to intact animals. The authors conclude that visual signals are rerouted to subserve function-
ality when the lesion is made at 1 month of age, but not at 1 day of age.
Keywords: brain damage, early lesion, visual system, animal model, neuroplasticity
The degree to which brain damage affects behavior depends on
the developmental period in which the lesion occurs: Lesions made
earlier in life often have better functional outcomes than equivalent
lesions sustained in adulthood. The basis of this difference is
thought to be the neuroplastic ability of the young brain to pur-
posely rewire circuits and systems to functionally bypass a lesion
(Chugani, Muller, & Chugani, 1996; Payne & Lomber, 2001).
Age-at-lesiondependent sparing of function has been demon-
strated specifically for motor cortex (Kennard, 1936, 1938), pre-
frontal cortex (Goldman, Rosvold, & Mishkin, 1970; Kolb, 1987),
and visual cortex (Shupert, Cornwell, & Payne, 1993), as well as
for large unilateral cortical lesions (Villablanca, Burgess, &
Olmstead, 1986; Whishaw & Kolb, 1988). However, the capacity
of the young brain to recover well from lesion is not assured.
Indeed, experimental work has shown that an early lesion does not
guarantee a higher degree of recovery and in fact may be more
debilitating to function than a late lesion (Anderson, Catroppa,
Morse, Haritous, & Rosenfeld, 2005; Kolb, 1987; Kolb & Coie,
2000; Kolb & Gibb, 2007; Villablanca & Hovda, 2000).
The cat is one of the most studied models of infant-lesion
induced cerebral reorganization and sparing of function (Payne &
Lomber, 2002; Spear, 1995; Villablanca, Schmanke, & Hovda,
1999) and has been used to demonstrate that lesions of primary
visual cortex at postnatal day 1 (P1) produces rewiring of visual
circuits (Kalil, Tong, & Spear, 1991; Lomber, MacNeil, & Payne,
1995; Lomber, Payne, Cornwell, & Pearson, 1993; Payne &
Lomber, 1998) and alterations in their metabolic capacities and
physiological properties (Desautels & Casanova, 2001; Guido,
Spear, & Tong, 1992; Ouellette, Minville, Boire, Ptito, &
Casanova, 2007; Spear, Tong, & McCall, 1988); overall, this
reorganization serves to produce a blurring of the ordinarily sharp
cerebral localization of function (Lomber & Payne, 2001) and
correlates with a higher degree of functional recovery in P1-
lesioned animals than in adults with equivalent brain damage
(Hovda & Villablanca, 1990; Payne, 2003; Payne & Cornwell,
1994).
However, even as the P1-lesioned animals are able to invoke
plasticity for the purposes of rerouting visual circuits and produc-
ing better performance in visually guided tasks than animals with
equivalent lesions made in adulthood (Hovda & Villablanca, 1990;
R. Jarrett Rushmore, Laura Rigolo, Amanda K. Peer, Linda M. Afifi,
and Bertram R. Payne, Laboratory of Cerebral Dynamics, Plasticity, and
Rehabilitation, Department of Anatomy and Neurobiology, Boston Uni-
versity School of Medicine; Antoni Valero-Cabre, Laboratory of Cerebral
Dynamics, Plasticity, and Rehabilitation, Department of Anatomy and
Neurobiology, Boston University School of Medicine, and TREAT Vision
and Department of Neurology, Fondation Ophtalmologique Rothschild,
Paris, France.
This work was supported by Grant NS33975 to Bertram R. Payne. We
gratefully acknowledge the technical support of Meghan Clancy, Kim
Song, Chad Rusthoven, Divya Manoharan, Jessica Arista, Jennifer Tadros,
and Jennifer Johnson. Julie Sandell and Donald Mitchell provided valuable
advice during the project. Margaret MacNeil and Leah Schweid provided
valuable comments.
Correspondence concerning this article should be addressed to R. Jarrett
Rushmore, Department of Anatomy and Neurobiology, Boston University
School of Medicine, 700 Albany Street, W702, Boston, MA 02118. E-mail:
rushmore@bu.edu
Behavioral Neuroscience Copyright 2008 by the American Psychological Association
2008, Vol. 122, No. 6, 12741283 0735-7044/08/$12.00 DOI: 10.1037/a0013586
1274
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Payne, 2003; Payne & Cornwell, 1994; Shupert et al., 1993), the
same capacity may also make cerebral networks more susceptible
to the induction of maladaptive sequelae. In cats with lesions of
primary visual cortex at P1, not only do the cells in the dorsal
division of the lateral geniculate nucleus undergo severe retrograde
degeneration (Tumosa, McCall, Guido, & Spear, 1989), but cells
in the retina also die. The transneuronal retrograde degeneration
suffered by retinal ganglion cells is specific for beta retinal gan-
glion cells (Payne, Pearson, & Cornwell, 1984; Tong, Spear, Kalil,
& Callahan, 1982), which have small receptive fields and encode
signals of high spatial frequency (Cleland, Harding, & Tulunay-
Keesey, 1979; Enroth-Cugell & Robson, 1966). After P1 lesion,
90% of beta retinal ganglion cells die (Payne et al., 1984; Tong et
al., 1982).
In a fully developed system, the loss of the beta ganglion cell
complement would impose strict limits on the capacity to encode
and process visual stimuli of high spatial frequency. In a devel-
oping system capable of extensive adaptive neuroplasticity, how-
ever, it is unclear whether the potential to rewire circuits can
overcome the depletion of the beta retinal ganglion cell array to
subserve function.
We assessed this interaction by quantitatively measuring the
capacity of early-lesioned animals to discriminate visual stimuli on
the basis of spatial frequency content. If age-dependent lesion
mechanisms in P1-lesioned cats are sufficient to overcome the
effects of transneuronal retrograde degeneration of beta cells, we
would expect to observe functional sparing and consequent high
levels of performance on the acuity-based task. For comparison,
two groups of cats with equivalent lesions of primary visual cortex
were tested. One group underwent lesion at 1 month of age (P28);
these cats maintained high levels of age-dependent neuroplasticity
but did not undergo transneuronal retrograde degeneration of ret-
inal ganglion cells (Theoret, Boire, & Ptito, 1997; Payne &
Lomber, 1998). The other group underwent lesion at adulthood
(180 days); this group was characterized by an intact beta-cell
array, but did not exhibit neuroplastic reorganization. Overall, a
comparison between these groups permits an assessment of the
interaction between levels of adaptive neuroplasticity and the
impact of beta retinal ganglion cell degeneration.
Materials and Method
Subjects
All cats were obtained from a licensed cat breeder (Liberty
Laboratories, Waverly, NY, or Harlan, Indianapolis, IN) or were
born from pregnant dams obtained from the same source. Cats
were divided into four groups: intact cats (Group A), cats that
sustained a lesion of primary visual cortex at P1 (Group B), cats
that received an equivalent lesion at 1 month of age (P28; Group
C), and cats that received a lesion of primary visual cortex in
adulthood (180 days; Group D). All cats were female, except for
1 cat in the P1 group (Cat B1) and 1 in the P28 group (Cat C2).
With the exception of the 2 animals in the C group, all cats were
taken from different litters. Cats were housed with a 12:12 light
dark cycle and were fed ad libitum for 1 hr each day. Cats were not
food or water deprived during the behavioral training or testing.
All procedures were approved by the Institutional Animal Care
and Use Committee of Boston University School of Medicine and
in accordance with the Guidelines for the Care and Use of Mam-
mals in Neuroscience and Behavioral Research (Van Sluyters et
al., 2001).
Surgical Procedures
Primary visual cortex (areas 17 and 18; Payne & Peters, 2002)
was removed bilaterally from cats at the day of birth (P1), at P28,
or in adulthood (6 months, P180), as described previously (Corn-
well & Payne, 1989; Lomber et al., 1993, 1995; MacNeil, Einstein,
& Payne, 1997; MacNeil, Lomber, & Payne, 1996; Payne &
Lomber, 1998; Payne, Lomber, & Gelston, 2000; Payne et al.,
1984). Lesions were made using sterile and aseptic technique.
Kittens were anesthetized with halothane (3% vol/vol) in 30%
oxygen and 70% nitrous oxide and were placed on a heating pad
to maintain normothermia. Heart and respiration rates were con-
tinuously monitored. The dorsal aspect of the skull was exposed
with a midline skin incision, and bilateral craniotomies were made
over the posterior occipital lobes to expose the primary visual
cortex. Areas 17 and 18 were removed by subpial aspiration, and
sterile gelatin sponges (Ethicon, Somerville, NJ) were placed in
the cortical defect and the durae was replaced. Bilateral lesions
were performed in one procedure in P1 kittens, but in two stages
in P28 kittens. At P28, a two-stage surgery was performed (one
hemisphere underwent surgery at P25, the other at P28; Cornwell
& Payne, 1989). In both groups, the incision was closed with
surgical staples, and the anesthesia was subsequently discontinued.
On waking, the kitten was placed back with the mother and closely
monitored. Broad-spectrum antibiotics (Ambipen, 0.1 cc im) and
the anti-inflammatory dexamethasone (1 mg/kg im) were admin-
istered daily for 1 week after the surgery. Wound clips were
removed 910 days after surgery. Kittens grew up with their
littermates and were moved to communal housing after weaning.
Cats began behavioral testing at approximately 1 year of age.
It is important to recognize two unavoidable confounds embed-
ded within this methodology. First, the neonatal brain is particu-
larly vulnerable to the effects of anesthesia, and it is likely that the
halothane administered during surgery produced a degree of cell
loss or otherwise altered cortical structure in the developing brain
(Kolb & Cioe, 2000; Jevtovic-Todorovic et al., 2003; Nunez &
Juraska, 2000); the degree of cell loss may have been different
between the P1 and P28 groups. Second, it should be acknowl-
edged that the two-stage nature of the surgery in the P28 animals
may have contributed in some way to the sparing of function.
Unfortunately, at this stage the parietal bone is undergoing vascu-
larization, and a two-stage surgery is required to minimize blood
loss and mortality in P28 cats (Cornwell & Payne, 1989). Overall,
it is unclear to what degree these two variables contribute to the
findings; therefore, the results of the study should be most parsi-
moniously interpreted in light of these two variables.
Adult cats (6 months old) were anesthetized with pentobarbi-
tal sodium (25 mg/kg iv) and placed in a stereotaxic frame.
Atropine sulfate (0.01 mg/kg sc), dexamethasone (1.0 mg/kg im),
and antibiotics (Cephazolin; 1020 mg/kg iv) were administered
before the procedure. Electrocardiogram, heart rate, respiration
rate, core temperature, and pedal reflexes were monitored to en-
sure depth of anesthesia. Craniotomies were performed over the
left and right marginal and posterior lateral gyri, the dura were
reflected, and the marginal and posterolateral gyri were removed
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SPARING OF ACUITY AFTER EARLY LESION
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via subpial aspiration and Gelfoam was placed in the defect. The
bone piece was replaced, muscle and skin were sutured, and the cat
closely monitored. Cats were given antibiotics (Cefazolin, 1020
mg/kg im) and dexamethasone (1 mg/kg im) for 5 days after the
surgery in decreasing dosages, and buprenorphine (0.0050.01 mg/kg
sc) was administered postoperatively in consultation with institutional
veterinary staff. Testing began 23 weeks after surgery.
Behavioral Procedures
Cats were trained in a two-alternative forced-choice task and to
discriminate between two gratings of equal spatial frequencies on
the basis of orientation: One grating was always horizontally
disposed (0), and the other was vertical (90).
For all assessments of behavior, a computer-controlled Penn-
sylvania General Testing Apparatus (PGTA) was used. The main
body of the PGTA consisted of a holding chamber that opened into
a decision area and led into two runways separated by a midline
divider (see Figure 1). Two monitors (17 in., or 43.2 cm; 1,024
768 pixels, 75-Hz refresh rate) that presented precisely calibrated
(Spyder with OptiCAL, Pantone Inc.) visual stimuli sat on a table
at the end of each runway. The mean luminance of the monitors
was 40 cd/m2, and a Macintosh G4 computer running Vista
software (Cerebral Mechanics, Lethbridge, Alberta; Prusky, West,
& Douglas, 2000) controlled stimulus presentation to both moni-
tors, determined the experimental setup, and collected data. The
apparatus was painted matte black to minimize reflection.
Each trial began with a cat being placed in the holding chamber,
which was closed on all sides to prevent the cat from viewing the
experimenters actions (see Figure 1). Two panels, one opaque and
the other transparent, were located at the end of the holding chamber
toward the runway and monitors. The opaque panel was lifted first to
allow the cat to view the runways and the contents of the monitors
through the transparent panel. After a variable delay, the transpar-
ent panel was lifted, and the cat was free to move into the decision
area of the apparatus. The decision area was a triangular-shaped
area that opened into two runways, which were separated from
each other by a 10.5-cm-high barrier and which each led to a
monitor. While in the decision box, the cat would typically look at
the contents of one monitor, then the contents of the other. The cat
would then make a decision to enter a runway and approach a
monitor. Each monitor was located 71 cm from the decision box;
when the front paws of the cat extended into the runway, the cat
was considered to have made a decision. The cat then walked
down the length of the runway and collected a food reward if she
chose the correct stimulus. The food reward was placed in a
shallow dish behind a small matte black barrier. The barrier neither
obscured viewing of the monitors nor allowed the cat to detect the
presence of the food reward. Barriers were present in front of both
monitors and both concealed dishes; only the dish corresponding
to the reinforced visual stimulus held a food reward. The food
reward was a small morsel of wet cat food (flavors: Ocean Fish,
Chicken, Beef, Chicken and Beef, Salmon, and Turkey; Triumph
Pet Industries, Red Bay, AL).
The cat was allowed to eat the food reward, was typically
verbally encouraged and handled, and was then returned to the
holding chamber for the next trial. If the cat chose the incorrect
runway, no food reward was given, and the cat was returned to the
holding box. No negative reinforcement was applied. While wait-
1
2
3 3
Figure 1. A drawing of the apparatus used to test the cats ability to
discriminate between stimuli. Each trial begins with the cat in the holding
box (1). The stimuli are presented on the monitors, and the opaque door is
lifted (solid arrows). After a variable delay, the transparent door is also
lifted (dashed arrows), and the cat emerges from the box into the triangular
area (2). The cat looks from one monitor to the other (dashed outline of
head) before making a decision and progressing down one of the runways.
If the stimulus corresponds to the rewarded stimulus (), the cat finds and
collects the reward behind an opaque lip (solid 3). If the cat chooses the
runway and monitor () with the unrewarded stimulus (dashed 3), the cat
is not rewarded. After the cat has entered one or the other runway with her
front paws, a decision is assumed to be reached, and the cat is not allowed
to go to the other monitor.
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RUSHMORE ET AL.
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ing for the next trial, the operator removed both reward dishes,
baited one, and replaced both in front of the monitors to prevent
the cat from detecting the correct monitor by hearing movement
from one runway or by any other nonvisual stimulusrelated cue
produced by selective baiting. Cats were tested five times a week.
Darkening Procedures
Once the cat was introduced and acclimated to the apparatus, the
next step was to introduce the demands of the task. The cat was
randomly assigned to either a horizontal or a vertical grating,
which was used as the positive and rewarded stimuli. The nonre-
warded, or negative, stimulus was the same stimulus as the posi-
tive stimulus, but rotated by 90. Thus, for a cat that had a
positive stimulus of a horizontal grating, the negative stimulus
consisted of a vertical grating. The positive stimulus for each
cat was a grating (spatial frequency 0.169 cycles per degree
[cpd]) with a 100% contrast between the light and dark bars of the
grating ([L
max
L
min
/L
max
L
min
], where L
max
and L
min
are the
maximum and minimum luminance values across the grating pat-
tern, respectively). Before testing began, the nonrewarded stimulus
was darkened by 98% to encourage the cat to progress to the
positive (and lighter) monitor and begin to associate the pattern
with a food reward. The choice of the positive stimulus was varied
in a predetermined sequence (LRLLRLRR, where L indicates that
the positive stimulus is on the left-hand monitor and R indicates
that the positive stimulus is on the right-hand monitor). Testing
consisted of blocks of 30 trials. Responses were recorded as
correct or incorrect. Criterion was set at 28 out of 30 correct trials;
if the cat achieved this performance, the next testing block was
applied with the darkness of the negative stimulus decreased by
1%. If the cat did not achieve criterion performance, the negative
stimulus was further darkened by 2%. Once cats achieved a condition
in which the negative stimulus was darkened by 90%, alterations in
darkness with behavioral performance changed in 5% increments.
The net result of these procedures was to train the cat to progressively
rely less on brightness cues and more on orientation cues.
Changing parameters of the visual stimulus with performance
was referred to as the staircase method; this method was used in all
procedures. Formal acuity testing began when the nonreinforced
stimulus was not darkened.
Visual Acuity Testing
After the darkening protocol, the sequence of stimuli was
changed to a pseudorandom sequence, and the criterion level was
altered to ascribe to a predetermined procedure; cats were consid-
ered to achieve criterion if they achieved 7 out of 10, 4 out of 5,
5 out of 6, or 3 out of 3 correct. If cats achieved criterion, the
spatial frequency of both the positive and the negative stimuli was
increased by 0.17 cpd. If cats failed to reach criterion (6 out of 10
or lower), the spatial frequency was decreased by 0.34 cpd. Three
failures ended the session for the day. Cats were begun at a spatial
frequency 1.0 cpd below the previous days peak performance.
Thus, the cats performance dictated the number of trials per day.
A cat was considered to have achieved plateau when perfor-
mance did not appreciably change over the course of a months
testing. In some cases, testing was extended to ensure plateau. A
subset of animals from each group were tested with visual stimuli
that had a Gaussian mask overlaid on the spatial frequency pattern
to exclude the possibility that the edge of the monitor was playing
a role in the ability to discriminate the visual stimuli. In all these
instances, cats achieved the same acuity as with the full-screen
grating.
Euthanasia and Tissue Processing
At the end of the experiment, cats were injected with heparin
(5,000 units) and sodium nitrite (1.5 cc of 1% solution) and were
given a final injection of sodium pentobarbital (120 mg/kg iv). The
brains were fixed via intravascular perfusion of aldehydes (1.25%
gluteraldehyde and 1% paraformaldehyde in 0.1 M phosphate
buffer, pH 7.4). Brains were removed, run though a series of
increasing concentrations of sucrose solutions (10%, 20%, and
30%), and cut into 52-m-thick sections on a freezing microtome.
Sections were mounted on gelatinized slides and processed for
Nissl substance.
Statistical Analysis
Behavioral results were compared by nonparametric analysis
using a MannWhitney U test. Comparisons were considered
significant if the p value was less than .05.
Results
Lesion Analysis
The lesions were largely complete, and the vast majority of
areas 17 and 18 was removed (Figure 2). Cortical sparing, when
A.
Cat D2
17
18
18
17
18
P180 P28
Cat C1
B.
Cat B2
P1
C.
D.
Figure 2. Lesion reconstructions. Drawing of the cat brain to show
extents of lesion. Dorsal and medial views for each brain showing the
extent of areas 17 and 18 (upper left) and lesion extent in representative
cases from each group. Adapted from Topographischer Hirnatlas der Katz
fur Experimentale Physiologische Untersuchungen [Topographic atlas of
the cat brain for experimental physiology research], by F. Reinoso-Suarez,
1961. Copyright 1961, with permission from Merck KGaA. P1 postnatal
day 1; P28 postnatal day 28; P180 postnatal day 180.
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present, was located in the inferior region of areas 17 and 18 on the
posterior splenial gyrus. This region corresponds to the upper
visual field representation and is consistent with the location and
extent of sparing observed in other studies in this system (Kaye,
Mitchell, & Cynader, 1981; Kruger, Muller-Kusdian, Kiefer, &
Berlucchi, 1988; Lomber et al., 1993, 1995; MacNeil et al., 1996;
Payne, 2003; Payne & Lomber, 1998; Payne et al., 2000). Minor
sparing of this cortex was present in most cats to varying degrees,
but degree of sparing within groups did not appear to covary with
behavioral performance, nor did any animal or group view the
stimuli in any fashion consistent with selective positioning of the
image on the upper field representation of the retina.
Behavioral Assays
Six intact cats were tested using a PGTA in a modified staircase
procedure (Figure 3). All intact cats achieved criterion on the
maximum acuity of the PGTA (9.98 cpd). In spite of the constancy
of the final acuity measure, cats exhibited tremendous variability
in performance. Some cats showed an incremental increase in
performance to maximum performance (Cat A1); others displayed
incremental or even plateau performance for some time, then
displayed very high and quick levels of performance to a second
plateau (Cat A4); and still other cats displayed a rise in performance
superimposed on oscillatory performance (Cats A2 and A6).
Four cats with bilateral lesions of areas 17 and 18 sustained on
P1 were tested to determine maximum acuity (Figure 4A). Peak
measures of acuity in the P1 group were significantly lower than
those of intact cats (P1 mean 4.65 0.86).
Two cats that received bilateral lesions of areas 17 and 18 at 1
month of age (P28 group) were tested for acuity (Figure 4B). Both
cats achieved the limit of acuity and were identical to the values
obtained by intact cats.
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Intact Cats
Figure 3. Performance of intact cats on the spatial frequency discrimination task. The complete acuity data set
is presented for each subject. Data points represent the peak acuity (cycles per degree) for each testing session.
Note that the abscissae are different for each graph.
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Three cats underwent lesions of primary visual cortex during
adulthood (Figure 5). Two of the cats had been previously tested
for acuity as intact animals (D1 A1 and D2 A4), and the third
cat (D3) learned the task after lesion. The levels of acuity they
were capable of discriminating were substantially and significantly
lower than those of the intact group (Figure 6A; P180 mean
3.27 1.07), but not significantly different from those of the P1
group. None of the groups were statistically different in the time it
took to reach their peak acuity (Figure 6B).
The intact cats that obtained lesions after acuity testing did not
retain the capacity to perform the task at high levels after lesion;
both Cats D1 and D2 had to begin at the lowest spatial frequency
and progressively advance.
Discussion
Cats with lesion of primary visual cortex in adulthood became
impaired in the acuity task and performance dropped from 9.98
cpd to 35 cpd. Cats that sustained lesion of primary visual cortex
at 1 month of age (P28) were unimpaired relative to intact cats and
demonstrated full sparing of function. This reflects a rerouting of
circuits around the lesion to mediate function. Surprisingly, cats
that underwent lesion at P1 did not exhibit any sparing of function,
and performance was not statistically different than cats with an
equivalent lesion sustained at adulthood. This result suggests that
P1-lesioned cats do not exhibit any sparing of acuity functions, and
neuroplastic mechanisms were insufficient to overcome the retinal
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A. P1 Cats
B. P28 Cats
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Figure 4. Performance of early lesion (postnatal day 1 [P1] and postnatal day 28 [P28]) cats on the spatial
frequency discrimination task. Graph conventions are the same as in Figure 3.
1279
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sequelae of maladaptive lesion-induced plasticity. These data in-
dicate that the impact of brain damage at different times in devel-
opment may result in drastic changes in outcome.
Intact Performance
The intact cats were all able to discriminate gratings close to 10
cpd, a level higher than previously reported and that corresponds
to theoretical predictions of maximum acuity on the basis of
ganglion cell arrays (Cleland, Crewther, Crewther, & Mitchell,
1982; Cleland et al., 1979; Hughes, 1981; Wassle, Boycott, &
Illing, 1981). As first reported by Hall and Mitchell (1991), a
period of pseudoplateau performance was observed in some cats
(see Cat A4, Figure 3) in which the daily maximum acuity was
found to be relatively constant. At a certain point, the peak spatial
frequency changed, and the cats were able to correctly discriminate
gratings at a substantially higher spatial frequency. The peak
spatial frequency exhibited substantial oscillation over time, and
different cats demonstrated different patterns of performance. Both
of these factors likely contributed to the historical underestimation
of cat acuity measures (see Hall and Mitchell, 1991, for a sum-
mary) and the previous discordance between the grain of cat beta
retinal ganglion cell arrays and behaviorally-derived measures of
visual acuity.
Testing Session Number
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Cat D3
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P180 Cats
Figure 5. Performance of adult-lesioned (postnatal day 180 [P180]) cats
on the spatial frequency discrimination task. Graph conventions are the
same as in Figure 3.
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p<0.05 p<0.05

Figure 6. Group means and time-to-peak measures. A: Average spatial
frequency for cats with lesions sustained at postnatal day 1 (P1; n 4),
postnatal day 28 (P28; n 2), and adulthood (postnatal day 180 [P180];
n 3) and for intact cats (Intact; n 6). The maximum acuity from the
P1 and P180 groups were significantly different from intact values. B:
Average number of testing sessions to reach peak acuity in lesion groups
and intact groups. No difference was found between the groups. For both
A and B, values represent the group mean, and error bars represent the
standard error of the mean.
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Cats With Lesions
In adult cats, bilateral lesion of areas 17 and 18 produced a drop
in acuity from approximately 10 cpd to 25 cpd. These data
suggest that the integrity of primary visual cortex is critical for the
ability to discriminate visual stimuli on the basis of high spatial
frequency content (5 cpd). These data are consistent with pre-
vious studies showing that lesion of primary visual cortex results
in a loss of spatial frequency-dependent discrimination capacity
(Mitchell, 1990; Pasternak & Maunsell, 1992; Pasternak, Tomp-
kins, & Olson, 1995). Moreover, the data support the view that
primary visual cortex is the exclusive site of entry of X signals to
the cerebral cortex (Payne & Peters, 2002). A lesion of this cortex,
therefore, disconnects the X signals from processing. The X sig-
nals in P180-lesioned cats are still generated by beta ganglion cells
in the retina and transmitted to the lateral geniculate nucleus, but
retrograde degeneration of geniculate X cells pursuant to the visual
cortical lesion ensures no further relay to other brain structures.
A point of interest in the adult-lesioned cats is the maintenance
of low levels of spatial frequency discrimination ability in the
absence of primary visual cortex. As noted above, it is unlikely
that the X stream remains connected to cortex after lesion of
primary visual cortex. The Y stream, carried by alpha ganglion
cells, is the most likely candidate to relay these signals; alpha
ganglion cells in the area centralis respond to spatial frequencies of
up to 4 cpd (Cleland et al., 1979, 1982) and would be well suited
to subserve the level of acuity function observed in this study.
However, the Y stream is unlikely to be fully intact in adult-
lesioned animals because area 18 is the dominant cortical site of
entry of Y signals. Unlike the X stream, however, Y input also
reaches cortex in other ways: (a) Alpha ganglion cell axons project
collaterals to the superior colliculus, and from here the Y stream
may reach extrastriate cortices by synapsing with neurons in
extrageniculate thalamus (Abramson & Chalupa, 1988), and (b) a
subset of geniculate neurons maintains collateral projections to
extrastriate regions. The similarity in the levels achieved by P180-
lesioned cats and the pseudoplateau levels of intact animals sug-
gests that the Y stream may underlay analysis of low to moderate
spatial frequencies in the intact animal. It should be noted, how-
ever, that the alpha retinal ganglion cell array is a minority (about
10%) of retinal ganglion cells, and as such the residual acuity
function in P180-lesioned cats must either be carried out by a small
sensory array or in conjunction with signals from sluggish or
gamma retinal ganglion cells, some of which carry signals that
respond to acuities rivaling those carried in the Y stream (Cleland
et al., 1979, 1982).
In the P1-lesioned cats, a similar level of behavioral perfor-
mance was found, but the substrate is likely to be fundamentally
different. In these animals, one might expect that the high potential
for the system to undergo neuroplasticity would effect a rewiring
of circuits around the lesion to other cortical areas (Payne &
Lomber, 1998) and give remaining visual cortex access to X-type
signals and produce a higher degree of function (e.g., Payne &
Lomber, 2002). In P1-lesioned cats, rewiring of Y and W signals
to extrastriate regions, particularly to the middle suprasylvian area,
has been well documented (Kalil et al., 1991; Lomber et al., 1995;
MacNeil et al., 1997; Payne & Lomber, 1998). However, this
intrinsic neuroplastic ability is countered by the transneuronal
retrograde degeneration of beta retinal ganglion cells (Payne et al.,
1984; Pearson, Labar, Payne, Cornwell, & Aggarwal, 1981; Tong
et al., 1982). Beta retinal ganglion cells relay signals of high acuity
and are concentrated at the area centralis, which serves as the
center of the cats optical axis (Boycott & Wassle, 1974; Enroth-
Cugell & Robson, 1966; Stein, Johnson, & Berson, 1996; Stone,
1983); regardless of the brains capacity to engage adaptive plas-
ticity and reroute visual signals to candidate areas, the diminished
density of the beta retinal ganglion cell array appears to place a
fundamental limit on the ability of P1 cats to discriminate visual
stimuli on the basis of high spatial frequency content. The data
from the P1-lesioned cats suggest that no other retinal or cerebral
circuits take over the function of this high-acuity pathway and that
signals of high acuity are not spared. Although the P1-lesioned cats
and the adult-lesioned cats achieved the same levels of function,
the loss of the cortex in the adult-lesioned cats contributed to the
loss of function, whereas in the P1-lesioned cats, the reduced beta
ganglion cell array imposed functional limitations on the system.
The P28-lesioned group did not undergo transneuronal retro-
grade degeneration of beta retinal ganglion cells (Payne &
Lomber, 1998), and the retina maintained the ability to gather and
relay high-acuity signals to the brain (Mitchell, 1990). Our data
suggest the P28-lesioned group was able to take advantage of
inherent age-dependent neuroplastic processes to reroute these
signals to alternate brain areas (Payne & Lomber, 1998), which
presumably receive and process signals of high acuity and enable
sparing of acuity functions. As a result, the neuroplastic potential
inherent in P28-lesioned cats in conjunction with the normal beta
retinal ganglion cell array enabled complete sparing of function.
The precise postnatal interval in which the acuity function is
relocated is as early as P10 (Mitchell, 1990), but elaboration of the
precise extent of the window and the mechanisms that enable
sparing of function at P28 but not P1 requires more work.
Conclusions
These data indicate that a high level of sparing after lesion is
present if the concordance between neuroplastic potential and
circuitwide stability is at a maximum. The P1 cat is thought to be
equivalent to human embryonic week 2426 and the P28 cat is
equivalent in maturational status to a newborn human (Leonard &
Goldberger, 1987a, 1987b). The current data suggest that the
neuroplastic potential associated with the P1 stage does not confer
functional advantage after lesion, whereas equivalent brain dam-
age sustained at a slightly later point in development takes advan-
tage of both the stability of the emerging system and its neuro-
plastic potential to maximize the systems functional capacity.
Therefore, brain damage in infancy may permit excellent rerouting
of function and excellent behavioral outcomes if it co-occurs
during the appropriate developmental events. Seen from another
perspective, the same lesion sustained at different timepoints pro-
duces broadly different cerebral systems and brains, depending on
the developmental time of damage. These systems develop unique
anatomical and physiological characteristics and have very differ-
ent potentials for subserving specific functionalities. Future work
will determine whether neurorehabilitation during the immediate
postlesion interval would further increase the neuroplastic and
functional potential of these modified cerebral systems.
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Received April 30, 2008
Revision received June 10, 2008
Accepted June 26, 2008
1283
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