|Molecular Vision 2006;
Received 17 April 2004 | Accepted 12 April 2006 | Published 7 August 2006
Pre- and post-critical period induced reduction of Cat-301 immunoreactivity in the lateral geniculate nucleus and visual cortex of cats Y-blocked as adults or made strabismic as kittens
Zheng Qin Yin,1,2
Sheila G. Crewther,2,3
David P. Crewther2,5
1Southwest Eye Hospital/Southwest Hospital, Chongqing, China; 2School of Optometry, University of New South Wales, Sydney, Australia; 3School of Psychological Science, La Trobe University, Melbourne, Australia; 4Department of Anatomy and Histology, Institute for Biomedical Research, The University of Sydney, Sydney, Australia; 5Brain Sciences Institute, Swinburne University of Technology, Hawthorn, Australia
Correspondence to: Zheng Qin Yin, MD, PhD, Director & Professor of Southwest Eye Hospital, Director of Eye Bank, Director of Chongqing Institute of Retina, Southwest Hospital, Chongqing, 400038 People's Republic of China; Phone: 86-23-68754401(O); FAX: 86-23-68753686(O); email: email@example.com
Purpose: To test the post-critical period stability of perineuronal nets by comparing the expression of antigens on aggrecan (a chondroitin sulfate proteoglycan (CSPG) recognized by the monoclonal antibody Cat-301) in the lateral geniculate nucleus (LGN) and striate cortex (A17) of adult Y-blocked cats and cats made strabismic and amblyopic as kittens. The comparison tested the idea that pre- and post-critical period loss of synchronous activity would differentially affect the perineuronal net of Y-type neurons in LGN and A17.
Methods: Seven adult cats, two normal, three convergent strabismic amblyopic, and two monocularly Y-blocked cats, were used in this study. The strabismic amblyopic cats had been made monocularly esotropic (by tenotomy) at 14 days of age. The Y-block was created acutely by a pressure cuff placed on the optic nerve behind the left eye in adult cats. The efficacy of both procedures was tested electrophysiologically. Frontal frozen sections were incubated with the Cat-301 antibody and the labeling visualized using a DAB kit. The sections were counterstained with cresyl violet. In each section, Cat-301-stained cells with well-defined nucleoli were counted under a 20x objective with a computer-based quantitative microscope image analysis system.
Results: The percentage of positively labeled cells was reduced in LGN laminae that received input from the deviated eye in amblyopic cats and from the pressure-blocked eye in Y-blocked cats compared with normal cats. Surprisingly, the non-blocked laminae of the Y-blocked cats also showed a significant reduction in positively labeled neurons when compared to normals or to strabismic cats. In the visual cortex of both hemispheres of strabismic and Y-blocked cats, the density of immunopositive neurons was significantly reduced compared with normal. The effect was most pronounced in layers IV-VI for Y-blocked cats and in layer IV for strabismic amblyopic cats.
Conclusions: The results demonstrate that surface expression of aggrecan in adult cat LGN and A17 of adult cat is reduced both by chronic developmental loss of synchronous input from the two eyes and by acute changes in synchronous input in adulthood. Thus both pre- and post-critical plasticity in the expression of epitopes of aggrecan can be demonstrated. The uniform distribution of Cat-301 labeling tangentially within cortical layers of strabismic amblyopic cats indicates that the reduction in immunoreactivity observed with strabismus induced early in life is not simply eye-specific. Indeed, comparison of the immunopositivity of Y-blocked and strabismic animals, both in LGN and cortex, suggests that even after the critical period is ended, the physical removal of monocular Y-type afferent activity and weakening of binocular feedback connections between cortex and thalamus can alter the stability of the perineuronal nets surrounding the affected neurons.
Visual information is carried in anatomically and functionally separate parallel channels from the retina through thalamus to the striate visual cortex (A17) in mammals. In cats, these channels are derived from the three major retinal ganglion cell types (X, Y, and W) which have been characterized anatomically and physiologically in the retina and whose termination sites in the dorsal lateral geniculate nucleus (LGN) of the thalamus have been well-studied [1,2]. The central projections of the visual pathways of the cat mature during the first 3-4 postnatal months, "the critical period of visual development" , when the structure and function of visually responsive neurons are more susceptible to influence by the animal's visual experience. It has also been shown that the biochemical events that underlie the anatomical and functional progression of visual development and maturation of perineuronal nets (PNNs) may in fact dictate the parameters of critical periods in the visual pathway [4,5]. This has been demonstrated with monoclonal antibodies specific for chondroitin sulfate proteoglycans (CSPGs) associated with the surface of cell bodies and proximal dendrites of specific subsets of the mammalian CNS, including the Y cells in the cat LGN [6,7] and visual cortex . More recently a specific CSPG-aggrecan, has been identified that is recognized by the antibodies Cat-301, Cat-315 and Cat-316 .
Cat-301 has been reported to be first expressed on cells in the LGN around 4-5 weeks of age following normal visual experience, with the number of Cat-301-positive cells increasing gradually to adult levels of expression at about six months of age . Other evidence also demonstrates coincidence of the increase in the Cat-301 sensitive proteoglycan and the end of the critical period for neuronal plasticity . CSPGs have also been shown to be inhibitory to axonal sprouting into the perineuronal nets of the extracellular matrix surrounding the maturing synapses  towards the termination of the critical period, leading to the suggestion of a role for CSPGs and PNNs in maintaining synaptic stability and preventing plasticity in the mature animal .
Early dark rearing (DR) and monocular deprivation have been reported to markedly reduce Cat-301 immunoreactivity in the cat LGN and visual cortex [8,9,12]. We have also published a preliminary report of reduced Cat-301 labeling in the feline strabismic amblyopia model . This procedure of surgical misalignment in kittens results in permanent severe reduction in binocularity of neurons, amblyopia, but not visual deprivation, per se . Biochemical damage to the perineuronal net via degradation of CSPGs with chondroitinase-ABC has also been shown to induce post-critical period plasticity in adult rats  leading to suggestion that the mature extracellular matrix is "inhibitory for experience-dependent plasticity." Such results raise the possibility that direct interference with the integrity of the Y-pathway in adult cats by pressure block of the optic nerve may also induce post-critical changes [16,17]. The acute physiological effects of this Y-block technique in adult cats include minor changes to receptive field properties of neurons in Areas 17 and 18 and a marked shift in ocular dominance away from the Y-blocked eye in Area 18 [18,19] which receives a major direct Y input.
As the Cat-301 monoclonal antibody to aggregan has been considered to be selectively expressed on Y-type neurons of the visual pathway, the Y-block technique can be used to investigate whether neurons in the LGN or primary visual cortex, which receive input via the pressure-blocked optic nerve ('Y-blocked eye') would show decreased expression of CSPGs on the perineuronal net, or whether such expression is fixed towards the end of the developmental critical period. Thus, the purpose of the present study was to investigate stability of Cat-301 immunoreactivity in adulthood following a blockade of the Y-pathway in adult cats, and compare this to immunoreactivity in normal adult cats and to adult strabismic amblyopic cats after early misalignment of the visual axes as young kittens.
Animal and tissue preparations
Seven adult cats, two normal, three convergent strabismic, and two Y-blocked cats, were used in this study. The left eyes of the strabismic amblyopic cats were made monocularly esotropic (by tenotomy of the abducens muscle)  under general anesthesia at 14 days of age, and the kittens grew up with a pronounced squint measuring from 15 to 20°. After muscle section, the eyes were not surgically fixed but were maintained in place by a small amount of post-operative swelling. Physiological amblyopia was confirmed shortly before recording by multifocal visual evoked potential (mfVEP) measurements (VERIS, Electro-Diagnostic Imaging, San Francisco, CA).
Acute monocular blockade of Y-axons in two adult cats was produced by a procedure that has been described more fully previously [17,19]. Each animal was initially anesthetized deeply. The left optic nerve was exposed by a dorsal approach to the orbit, and a pair of electrodes was attached to the nerve just behind the eyeball. The pressure device (essentially a pressure cuff) was placed a few millimeters distal to the electrodes and the eyeball. A pair of bipolar electrodes was implanted into the contralateral optic tract. Stimulating the optic tract via the implanted electrodes and recording the field response of the optic nerve beyond the pressure-blocked region allowed the effect of the pressure-block to be monitored after the surgery. Conduction blockade has been shown to be maintained for more than three weeks . In the case of the animals in the current experiment, verification recordings took place the next day after the Y-block operation.
Prior to death, animals were deeply anesthetized with a lethal dose of Nembutal (100 mg/kg, intraperitoneal) and were perfused transcardially with 0.9% saline in 0.1 M phosphate buffer (PB) at pH 7.4 followed by cold fixative solution containing 4% paraformaldehyde in 0.1 M PB. Frontal frozen sections (20 μm) were mounted on gelatin-coated slides and were stored at -70 °C. Animal rearing and conduct of the experiments was in accordance with the Australian NH&MRC guidelines and the ARVO convention on animal use.
Details of the production and use of Cat-301 have been described elsewhere [6,21], wherein electron microscopic immunohistochemistry showed that Cat-301 labeling was specific to the surface of a sub-population of neurons (the perineuronal net). CAT 301 was the gift of Prof. Susan Hockfield. Sections were incubated overnight in Cat-301 antibody (undiluted) with 2% Triton X-100. The Cat-301 antibody was visualized using a DAB kit (ZYMED Laboratories, San Francisco, CA), which employs a biotinylated secondary antibody linked to an avidin-biotinylated-horseradish peroxidase (HRP). Representative sections were counterstained with cresyl violet. It should be noted that Nissl staining can mask low-levels of immunoreactivity, and hence Nissl counterstained sections actually bias any counting procedure towards the most heavily labeled cells. To control for nonspecific immunoreactions, a number of slides was processed for each experiment as described above, using IgE as the primary antibody. The evidence for antibody specific staining and tissue integrity of the Y-block cats are detailed below. It should also be noted that individual cells which show positive immunoreactivity can be well visualized for counting under the microscope at high power, with the Cat-301 antibody staining the perineuronal network brown, easily distinguishable on a chromatic basis from blue-purple of the cresyl violet counterstaining the Nissl bodies in the nucleus and cytosol (Figure 1). At low power it is much harder to discriminate the antibody staining from the Nissl counter stain and the cell specific antibody staining from background antibody product.
Cat-301 Immunostaining control procedures
Control procedures were carried out to ascertain the specificity of antibody staining. The results of such control tests for the Y-block cats are shown for the LGN in Figure 2 and for the cortex in Figure 3. The LGNs showed virtually no DAB product when IgE is used as the primary antibody (Figure 2A,B) but the expected perineuronal staining when the Cat-301 primary antibody was used (Figure 2C,D). Tissue integrity is good as demonstrated by the Nissl stained control section (Figure 2E,F). Similarly in cortex, the control IgE product shows no labeling associated with neurons (Figure 3A,B) whereas the uncounterstained Cat-301 product, shown at three magnifications (Figure 3C-E) clearly demonstrates the perineuronal staining characteristic of Cat-301 (arrows in Figure 3E) and furthermore highlights the preponderance of staining profiles in the upper layers (II-III) of visual cortex.
Cells with well-defined cresyl violet stained nucleoli in lamina A or A1 of the LGN were counted under a light microscope with a computer-based quantitative image analysis system (20x objective magnification with a field of view 200x200 μm) and designated as Cat-301 labeled or unlabeled. The first three fields of view under the microscope, of each section, when moving the stage from medial to lateral in LGN lamina A and lamina A1, were counted. The locations corresponded to visual-field eccentricities of 0° to 5°, 5° to 15°, and 15° to 45°, all within the binocular visual field . Monocular visual fields were also examined by taking two fields of view of each section through laminae A at 45° to 90° visual field eccentricity, for analysis.
For the LGN analysis, 36 transverse whole-brain sections containing the LGN from both hemispheres were analyzed in toto, six from each of the two normal animals, six each from the three strabismic animals and three from each of the two Y-blocked cats (both of which had the left optic nerve blocked). In the primary visual cortex, whole transverse sections covering the radial extent of both cortices were analyzed by using three microscope fields of view (20x objective magnification with a field of view 200x200 μm) located sequentially in layers II-III, IV and V-VI. Three such strips were analyzed for each hemisphere of each slide (chosen at random). Thirty-six brain sections were analyzed in toto, six from each of the two normal animals, six from each of the three strabismic animals and three from each of the two Y-blocked cats. As with the LGN, cells with well-defined cresyl violet stained nucleoli were counted and designated as Cat-301 labeled or unlabeled.
Two experienced histologists performed the counts; of these, one was unaware of the experimental source of the slides. Statistical comparison between samples of labeled neurons from strabismic, Y-blocked, and normal cat was made using analysis of variance (ANOVA).
Cat-301 visualization of aggrecan antigen distribution is apparent in the LGN and visual cortex of a normal adult cat (Figure 1), and confirms previous reports  with Figure 1A showing that aggrecan is localized in the perineuronal net, around the somata and proximal dendrites in the LGN. In the visual cortex (Figure 1B), the antibody staining also outlines the cell body somata, proximal dendrites and axons of pyramidal cells as a perineuronal net. Similar morphological features have been described previously [7,23,24]. Low power micrographs (Figure 4) of the LGN of normal, strabismic and Y-block animals show that Cat-301 staining is normally found in laminae A, A1 and the dorsal C laminae, and particularly in the interlaminar zones, and in the medial interlaminar and the perigeniculate nuclei. At this magnification, laminar differences, as occur in the geniculate of monocular lid sutured animals , were not observed.
At a higher level of magnification (100x objective), in counterstained material where the level of background staining is diminished, the staining around the somata is clearer and the pattern of staining shown in Figure 1 is observable on many of the somatic profiles. The proportion of somata with perineuronal staining (Figure 4C) appears higher in the normal animals compared with either the strabismic or Y-block animals (Figure 4F,I).
In striate cortex, greater immunopositive staining was seen in all layers for the normal cats compared with strabismic or Y-blocked cats (Figure 5A,C). Tangentially, along layer IV, there was little indication, either at the somatic or nonsomatic labeling level, of systematic variation in density of labeling that might have reflected differences in ocular dominance between the experimental and fellow eyes of the strabismic cats. Similarly, for the Y-block cats, while the staining density was obviously less than normal, there was no indication of systematic spatial variation along single layers (Figure 5). Comparison of Figure 5A,C,E show a clear difference in perineuronal labeling between outer cortex (layers II/III), where clear labeling of neurons is observed in all three conditions, to layer IV, where a reduction in immunopositive labeling is clear in both strabismic and Y-block sections, to layer VI, where labeling appears quite deficient in the Y-block figure (Figure 5E) compared with strabismic or normal (Figure 5A,C). However, despite the lower percentage of cells labeled, those that were labeled are clearly outlined, including details of the dendritic processes.
A total of 5893 cells were counted from the LGN of normal, strabismic amblyopic and Y-blocked cats. As noted previously in normal and strabismic cat, the percentage of cells labeling immunopositively to Cat-301 was always higher in layer A1 than in layer A. This was also true in the Y-blocked animals.
There was no significant difference (p>0.05) in positive labeling found between the laminae driven by the nondeviating eye of strabismic amblyopic cat and normal cat, though there is an obvious marked reduction in the number of positively labeled cells driven by the deviating eye of the strabismic cats compared with normal cats, either ipsi- or contralateral, (p<0.05; Figure 6). On the other hand, the percentage of cells positively staining for Cat-301 was markedly decreased in both LGN laminae of Y-blocked cats (i.e., receiving projections from either the Y-blocked or fellow eye) with significantly less immunolabeled neurons seen than in either the normal or strabismic amblyopic animals, (p<0.001; Figure 6).
A total of 12,901 cells were counted in the primary visual cortex of normal, strabismic amblyopic, and Y-blocked cats. The proportion of immunopositive cells in the various cortical layers of the three groups was calculated and are presented relative to the immunopositive level in the corresponding layers of normal cat cortex (Figure 7). Cat-301 labeled cells are densely distributed in 2 bands in layer III-IV and layer V-VI with individual cells labeled in upper layers II-III of primary visual cortex in normal cat. In both strabismic and Y-blocked cats, the percentage of Cat-301 immunopositive cells was reduced in layer IV, with fewer labeled cells in layer V-VI of Y-blocked cats compared with strabismic amblyopic and normal cats. Comparison of the distribution of immunopositive cells by cortical layer (Figure 7) showed lowered relative incidence in Y-blocked and strabismic cats compared with normal cats (p<0.001). In layer IV there was a pronounced reduction in the percentage of labeled cells in strabismic amblyopic and Y-block cats compared to normal (p<0.001). In layers V-VI, a significant difference was found between strabismic amblyopic and Y-blocked cats (p<0.001). In terms of the laminae most affected by experimental condition, layer IV was most affected in the strabismic amblyopic cats, while layer V-VI was most affected in the Y-block cats (Figure 7).
While the normal and strabismic cats showed patterns of Cat-301 immunoreactivity as previously reported [7,13], a marked reduction in immunopositive neurons in both the A17 of cortex and laminae A and A1 of the LGN of adult cats with acutely induced Y-block was observed. The results from the strabismic and Y-block cats show an overall effect qualitatively similar for the LGN to that seen in dark-reared cats , but differing in detail in cortex where the reduction of immunopositivity for dark-rearing was reported to be most pronounced in layers II/III and V/VI. Reduced levels of perineuronal immunoreactivity were seen in both LGN laminae whether receiving projections from the deviated or the nonstrabismic eyes or from Y-blocked and non-Y-blocked eyes, when compared to normals. Quantitative comparison of immunoreactivity in the primary visual cortex of normal and strabismic amblyopic cats indicates that the number of antibody-positive neurons was reduced primarily in layer IV, the major termination site of geniculate axons. For the adult Y-block animals, the most significant reduction in Cat-301 positivity was seen in layers IV and layers V-VI of primary visual cortex. As the perineuronal net is believed to stabilize by the end of the critical period [7,25] a reduction in immunopositive cells in adult Y-block cats was not expected, especially for laminae receiving input from the putatively normal fellow eye. Previous studies investigating distribution and density of Cat-301 label in adult cats monocularly deprived as kittens have shown a correlation between the loss of Y-afferents and a reduction in Cat-301 immunoreactivity in LGN and Visual Cortex . By contrast, adult cats (i.e., past the critical period) subjected to similar visual deprivation showed no reduction in Cat-301 expression  and no reduction in the number of functional Y-cells . Also, reverse suture for a period of six months in kittens reared to adulthood with monocular deprivation does not restore Cat-301 immunoreactivity to normal levels . However, post-critical period plasticity can be induced in adult rats following degradation of chondroitan sulfate proteoglycans .
Together, these results have been interpreted as the Cat-301 immunoreactivity in the LGN and striate cortex paralleling that of the experience-dependent physiological maturation of Y-cells. However, these earlier studies have been limited in their ability to differentiate between whether antibody expression in the adult is due to loss of activity throughout development or is a measure of current activity. The current study bypasses this problem by comparing antibody expression in adult cats made strabismic as young kittens, to adult cats within a week after exposure to a pressure-induced Y-block. The results demonstrate that under Y-block conditions, the level of Cat-301 immunoreactivity is still modifiable in post-critical period animals. It is acknowledged that there are direct physiological effects of Y-block including an acute reduction in axonal flow, changes in Area 17 and 18 receptive field properties, altered ocular dominance distributions and modified binocular properties [18,19,26]. Thus, it is possible that the post-critical period changes in immunoreactivity observed in the Y-block animals could be a reflection of the acute changes to the Y-system, as the anatomical material was obtained within one week of the Y-block procedure. However, the changes observed are more general than these direct effects, and hence require explanation.
The change in proportion of immunopositive cells in the LGN and cortex of the strabismic cats indicates that previous single cell physiological studies of LGN and cortex, which found a decrease in X-cell associated acuity in strabismic amblyopia [27-29] may reflect only a part of the total spectrum of neural alterations in strabismic amblyopia. A feature of the cortex of strabismic amblyopic cat is that the ocular dominance columns are much more electrophysiologically [28,30] and anatomically [31,32] distinct than those found in normal cat, presumably due to the long-term elimination of correlated activity between the two eyes and a reduction in the percentage of binocularly activated neurons. The absence of strong eye-related bands of Cat-301 labeling in strabismic cortex indicates that modifications in immunoreactivity of Y cells are not simply related to nonsynergistic early visual experience and the resultant amblyopia. Our results also suggest another explanation. Given the predominance of cortical feedback compared with retinal input to geniculate relay neurons, and the strongly binocular nature and nonlinear physiological properties of the Y-pathway, it is possible that the antibody staining reductions observed in both laminae of the strabismic and the Y-blocked cats are more related to the level of Y-generated activity in cortex at the time of sacrifice, given that the geniculate effects are also seen in the non-blocked laminae. A comparison of Figure 6 and Figure 7 show that the reduction in geniculate labeling is closely matched to the reduction in labeling in the deep layer of striate cortex (layer V/VI)-layers that signal directly back to superior colliculus and LGN, respectively, suggesting that the perineuronal net is at least partially under retrograde control. In normal cat, highly binocular layer VI neurons would normally project back to both laminae of the LGN. If control of the expression of CSPGs in LGN were related to the cortical source of input, a loss of binocular facilitation as occurs in strabismus, or abnormal binocular interaction as occurs in Y-block preparations may then be observable in laminae receiving input from an ostensibly normal eye.
We thank Professor Susan Hockfield of Yale University, New Haved, CT, who kindly supplied the Cat-301 antibody. We thank Professor Liam Burke and Bogdan Dreher of The University of Sydney, Sydney, Australia for the Y-block cats. A Chinese NSFC grant to Zheng Qin Yin (30025014) and an Australian NH&MRC grant (970539) to S. G. Crewther and D. P. Crewther supported this research.
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