118
NeuroscienceLetters, 119 (1990) 118-121 Elsevier ScientificPublishersIreland Ltd.
NSL 07267
Variations by layers and developmental changes in expression of telencephalin in the visual cortex of cat K a z u y u k i I m a m u r a , K e n s a k u Mori, Shogo Oka* a n d Y a s u y o s h i W a t a n a b e Department of Neuroscience, OsakaBioscienceInstitute, Osaka (Japan)
(Received 8 June 1990;Revisedversionreceived 13 July 1990;Accepted 16 July 1990) Key words: Telencephalin;Immunohistochemistry;Development;Striatecortex; Cat
The expressionof telencephalinin visualcortex of cat and monkeywas studied immunohistochemically.In adult cats and monkeys,immunoreactivity to a polyclonalantibodyraised against telencephalinwas especiallylow in layer IV, whichreceivesmassiveafferentinput from the thalamus. In kitten visualcortex, the antibodybound both layer IV and other cortical layersduring the most sensitiveperiod for ocular dominanceplasticity. Outside the sensitiveperiod, the stainingof layer IV was selectivelyreduced.These findingssuggestthat the expressionof telencephalinis developmentallyregulatedduring the earlypostnatal period and may play a role in regulatingplasticityduring the sensitiveperiod.
Cell surface molecules mediating cell-cell interactions play critical roles in the formation of neuronal architecture [2]. We recently identified and purified a novel membrane protein, telencephalin, which is expressed in the mammalian brain selectively by telencephalic neurons [10, 11]. The restricted distribution of telencephalin suggests that this membrane protein is most likely involved in functions specific to the telencephalic regions. Telencephalin is a glycoprotein and has a HNK-1 carbohydrate epitope (S. Oka et al., unpublished observation), which neural cell adhesion molecules share [3, 9, 12]. The expression of telencephalin is developmentally regulated and parallels synapse formation in time. These observations have suggested that telencephalin may be involved in cell-cell interactions in telencephalic regions. Previous immunohistochemical analyses have demonstrated that telencephalin is expressed in the gray matter of all regions of the telencephalon. However, in order to understand the functional roles of telencephalin, it is necessary to determine how its expression in specific regions of the telencephalon varies and to relate the expression pattern with the neuronal architecture in these regions. It is also necessary to study in detail the developmental changes of telencephalin expression in these regions. In the present study, we examined the variations by layers and developmental changes of telence*Present address: Shionogi Research Laboratories, Shionogi & Co. Ltd., Fukushima-ku,Osaka 553, Japan Correspondence: K. Imamura, Department of Neuroscience, Osaka BioscienceInstitute,6-2-4 Furuedai,Suita-shi,Osaka, 565 Japan. 0304-3940/90/$ 03.50 © 1990ElsevierScientificPublishersIreland Ltd.
phalin expression in the visual cortex. Visual cortex was chosen for study because knowledge of its functional organization, development and plasticity is extensive [e.g. 1, 4, 5], facilitating an understanding of the functional roles of telencephalin. Fourteen cats (1 week to 3 years old) were used for the present experiments. After receiving lethal overdoses of Nembutal (> 100 mg/kg), animals were transcardially perfused with 0.9% saline and 4% paraformaldehyde in 0.1 M phosphate-buffered saline (PBS, pH 7.4). Brain was postfixed overnight in the same fixative and the visual cortex was removed and soaked in 30 % sucrose in PBS until it sank. Other brain regions were used for other histochemical studies being carried out in our laboratory [8]. We also obtained occipital cortices from two adult male monkeys (Macaca fuscata fuscata, 8-9 kg). These animals had been used for other experiments carried out in our institute. Primary antibody (PAb) against telencephalin was obtained by immunizing mice with purified glycoprotein [11]. The procedures for immunostaining have been previously described in detail [8, 10, 11]. Briefly, 30/~m coronal sections were incubated with 0.03% Triton-X, then with 20% normal goat serum in PBS. Following several washes with PBS, sections were incubated for 2 h with polyclonal anti-telencephalin antiserum (1:100 dilution). Fluorescein isothiocyanate (FITC)-conjugated goat anti-mouse IgG was used as the second antibody. Neighboring sections were stained for cytochrome oxidase using Wong-Riley's protocol [13] or for Nissl substance with thionine. Fig. 1 compares anti-telencephalin antiserum (A),
119
IV V
Vl
I
II III
V VI
Fig. 1. lmmunofluorescence staining of the visual cortex with polyclonal antibody against telencephalin. A: a coronal section of the eat visual cortex (medial bank of the postlateral gyrus) was stained with the antibody. B: an adjacent section stained for cytochrome oxidase. C: thionine staining. D-F: corresponding sections from the monkey striate cortex. Lightly stained cytochrome oxidase blobs are indicated by arrows in E. Bar = 1 ram, Roman numerals, cortical layers. All of the regions shown are in area 17.
cytochrome oxidase (B) and Nissl staining (C) in the adult cat visual cortex. The white matter in the region of visual cortex was devoid of immunoreactivity to antitelencephalin antiserum (Fig. IA). In the gray matter, the antiserum faintly labeled layer IV, while intensely stained bundles of fibers were observed to perforate layer IV travelling toward the cortical surface. Cells of the other gray matter layers were intensely stained throughout except inside neuronal somata. In the section stained with cytochrome oxidase, a dense continuous band of high oxidative enzymatic activity was observed within layer IV (Fig. 1B). The neuropil within layers II, III and VI was moderately reactive. Layer V was distinguished for having a random distribution of highly reactive neurons against a rather light background. The expression of telencephalin is therefore significantly less pronounced in layer IV than in the other cortical layers, and in cat visual cortex it is complementary in distribution among the cortical layers to the expression of cytochrome oxidase. A similar relationship between the staining pattern for anti-telencephalin antiserum and
that for cytochrome oxidase was observed in monkey visual cortex (V1). The staining pattern achieved there with anti-telencephalin antiserum is shown in Fig. 1D. The white matter near the visual cortex was devoid of immunoreactivity, as was that of the cat. The immunoreactivity in layer IVa and IVc was quite low, although fine fiber processes in layer IVc were stained. The staining patterns in monkey V1 achieved with polyclonal anti-telencephalin antibody and with cytochrome oxidase were complementary, with the exception that immunofluorescence staining corresponding to cytochrome oxidase blobs was not found (Fig. 1D,E). Next, visual cortices of kittens of different ages were stained with polyclonal anti-telencephalin antibody in order to study postnatal developmental changes in staining (Fig. 2). In no brain examined was the white matter in the neighborhood of visual cortex labeled. In one week old kitten, immunoreactivity in the visual cortex was not pronounced, but blotchy regions of staining could be identified near the middle of the gray matter (Fig. 2A). A band of low immunoreactivity, possibly
120
Fig. 2. Developmentalchanges of immunofluorescencestaining of the cat visual cortex (medial bank of the postlateral gyrus, area 17) with antitelencephalinantibody. Coronal sectionswere obtained from postnatal 1-week-oldkitten (A), 3-week- (B), 5-week-(C), 7-week-(D), 9-week-(E), 13-week-(F), 17-week-old(G) and an adult (~3 years old) cat (H), respectively.Bar = 1 ram.
corresponding to that occurring in adult cortex, was observed also in the visual cortex of three week old kittens (Fig. 2B). Low immunoreactivity specific to layer IV was not clearly observable in the visual cortices of 5-, 7-, and 9-week-old kittens (Fig. 2C-E). Immunoreactivity in layer IV was relatively low in 9-week-old kitten (Fig. 2E) and was clearly lower there than in the other layers of the visual cortex of 13-week-old kitten (Fig. 2F). Low immunoreactivity in layer IV was also a conspicuous finding in 17-week-old kitten (Fig. 2G) and in adult cat (--~ 3 years old) (Fig. 2H). Previous studies have shown that telencephalin is expressed in the gray matter of all regions of the adult mammalian telencephalon, but not in non-telencephalic regions [10]. The present results demonstrate clearly that telencephalin expression varies by layer in the adult cat visual cortex. Specifically, immunoreactivity to telencephalin is considerably lower in layer IV than in other layers of the gray matter. Layers IVa and IVc in the monkey visual cortex also showed less immunoreactivity than other layers there. The diminished expression of telencephalin in layer IV was not specific to the visual
cortex but was observed also in several other regions of neocortex. This suggests that a basic pattern of telencephalin expression is common to all regions of the neocortex. Layer IV of the visual cortex receives massive inputs from thalamus. It has been shown in cat and monkey visual cortex that the termination sites of afferent fibers from the lateral geniculate nucleus correspond well to sites of dense cytochrome oxidase staining [6]. The present results have demonstrated that the sites of diminished expression of telencephalin coincide relatively well with those of intense cytochrome oxidase staining. This indicates that expression of telencephalin is decreased in those layers or sublayers in which massive thalamic afferent fibers terminate. These observations suggest that telencephalin expression on telencephalic neurons might be influenced by the massive afferent input from diencephalon. Observations relevant to the above have been made in the rabbit olfactory bulb [10]. In the adult bulb, expression of telencephalin has been shown to be diminished in the glomerular layer, in which olfactory nerve fibers
121 terminate massively on principal cells o f the bulb. Furthermore, a recent electron microscopic study has shown that telencephalin is not expressed by neurons which receive direct input f r o m olfactory nerve fibers (F. M u r a k a m i et al., personal communication). Considering these findings together with our own, it seems quite possible that the expression o f telencephalin is suppressed by massive direct afferents from non-telencephalic regions. The second m a j o r finding o f this study is that the expression o f telencephalin in cat visual cortex is developmentally regulated. It has already been reported that immunoreactivity against anti-telencephalin a n t i b o d y is barely detectable in m o s t regions o f the rabbit neocortex at birth, but increases during the early postnatal period [10]. In the present study, telencephalin has been shown to be present in all cortical layers o f cat visual cortex only between the age o f 4 to 13 weeks. Outside this time period, expression is substantially decreased in layer IV. The t e m p o r a l profile o f telencephalin expression in layer IV corresponds well to that o f the electrophysiologicallydefined sensitive period for visual cortical plasticity, including ocular d o m i n a n c e plasticity [7]. The results o f the present study suggest the intriguing possibility that the telencephalin m a y play a role in regulating ocular d o m i n a n c e plasticity. F u r t h e r studies will be necessary to test this hypothesis. We t h a n k Dr. M. C o n n o l l y for reading the m a n u s c r i p t and i m p r o v i n g the English. We also t h a n k Ms. N. M i k a jiri for secretarial service.
1 Blakemore, C., Maturation and modification in the developing visual system. In R. Held, H.W. Leibowitz and H.L. Teuber (Eds.), Handbook of Sensory Physiol., Vol. III, Springer, Berlin, 1978, pp. 377-436. 2 Dodd, J. and Jessell, T.M., Axon guidance and the patterning of neuron projections in vertebrates, Science, 242 (1988) 692-699. 3 Edelman, G.M., Cell adhesion molecules in the regulation of animal form and tissue pattern, Annu. Rev. Cell Biol., 2 (1986) 81116. 4 Frrgnac, Y. and Imbert, M., Development of neuronal selectivity in primary visual cortex of cat, Physiol. Rev., 64 (1984) 325-434. 5 Gilbert, C.D., Microcircuitry of the visual cortex, Annu. Rev. Neurosci., 6 (1983) 217-247. 6 Horton, J.C., Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex, Phil. Trans. R. Soc. Lond. Ser. B., 304 (1984) 199-253. 7 Hubel, D.H. and Wiesel, T.N., The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol., 206 (1970) 419-436. 8 Ikeda, J., Moil, K., Oka, S. and Watanabe, Y., A columnar arrangement of dendritic processes of entorhinal cortex neurons revealed by a monoclonal antibody, Brain Res., 505 (1989) 176179. 9 Kunemund, V., Jungalwala, F.B., Fisher, G., Cbou, D.K.H., Keilhauer, G. and Schachner, M., The L2/HNK-I carbohydrate of neural cell adhesion molecules is involved in cell interactions, J. Cell Biol., 106 (1988) 213-223. I0 Mori, K., Fujita, S.C., Watanabe, Y., Obata, K. and Hayaishi, O., Telencephalon-specific antigen identified by monoclonal antibody, Proc. Natl. Acad. Sci. U.S.A., 84 (1987) 3921-3925. 11 Oka, S., Moil, K. and Watanabe, Y., Mammalian telencephalic neurons express a segment-specific membrane glycoprotein, telencephalin, Neuroscience, 35 (1990) 93-103. 12 Pesheva, P., Horwitz, A.F. and Schachner, M., Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/ HNK-I and L3 carbohydrate structures shared by adhesion molecules, Neurosci. Lett., 83 (1987) 303-306. 13 Wong-Riley, M., Changes in the visual system of monocularly sutured or enucleated cat demonstrable with cytoehrome oxidase histochemistry, Brain Res., 171 (1979) 11-28.
NeuroscienceLetters, 119 (1990) 118-121 Elsevier ScientificPublishersIreland Ltd.
NSL 07267
Variations by layers and developmental changes in expression of telencephalin in the visual cortex of cat K a z u y u k i I m a m u r a , K e n s a k u Mori, Shogo Oka* a n d Y a s u y o s h i W a t a n a b e Department of Neuroscience, OsakaBioscienceInstitute, Osaka (Japan)
(Received 8 June 1990;Revisedversionreceived 13 July 1990;Accepted 16 July 1990) Key words: Telencephalin;Immunohistochemistry;Development;Striatecortex; Cat
The expressionof telencephalinin visualcortex of cat and monkeywas studied immunohistochemically.In adult cats and monkeys,immunoreactivity to a polyclonalantibodyraised against telencephalinwas especiallylow in layer IV, whichreceivesmassiveafferentinput from the thalamus. In kitten visualcortex, the antibodybound both layer IV and other cortical layersduring the most sensitiveperiod for ocular dominanceplasticity. Outside the sensitiveperiod, the stainingof layer IV was selectivelyreduced.These findingssuggestthat the expressionof telencephalinis developmentallyregulatedduring the earlypostnatal period and may play a role in regulatingplasticityduring the sensitiveperiod.
Cell surface molecules mediating cell-cell interactions play critical roles in the formation of neuronal architecture [2]. We recently identified and purified a novel membrane protein, telencephalin, which is expressed in the mammalian brain selectively by telencephalic neurons [10, 11]. The restricted distribution of telencephalin suggests that this membrane protein is most likely involved in functions specific to the telencephalic regions. Telencephalin is a glycoprotein and has a HNK-1 carbohydrate epitope (S. Oka et al., unpublished observation), which neural cell adhesion molecules share [3, 9, 12]. The expression of telencephalin is developmentally regulated and parallels synapse formation in time. These observations have suggested that telencephalin may be involved in cell-cell interactions in telencephalic regions. Previous immunohistochemical analyses have demonstrated that telencephalin is expressed in the gray matter of all regions of the telencephalon. However, in order to understand the functional roles of telencephalin, it is necessary to determine how its expression in specific regions of the telencephalon varies and to relate the expression pattern with the neuronal architecture in these regions. It is also necessary to study in detail the developmental changes of telencephalin expression in these regions. In the present study, we examined the variations by layers and developmental changes of telence*Present address: Shionogi Research Laboratories, Shionogi & Co. Ltd., Fukushima-ku,Osaka 553, Japan Correspondence: K. Imamura, Department of Neuroscience, Osaka BioscienceInstitute,6-2-4 Furuedai,Suita-shi,Osaka, 565 Japan. 0304-3940/90/$ 03.50 © 1990ElsevierScientificPublishersIreland Ltd.
phalin expression in the visual cortex. Visual cortex was chosen for study because knowledge of its functional organization, development and plasticity is extensive [e.g. 1, 4, 5], facilitating an understanding of the functional roles of telencephalin. Fourteen cats (1 week to 3 years old) were used for the present experiments. After receiving lethal overdoses of Nembutal (> 100 mg/kg), animals were transcardially perfused with 0.9% saline and 4% paraformaldehyde in 0.1 M phosphate-buffered saline (PBS, pH 7.4). Brain was postfixed overnight in the same fixative and the visual cortex was removed and soaked in 30 % sucrose in PBS until it sank. Other brain regions were used for other histochemical studies being carried out in our laboratory [8]. We also obtained occipital cortices from two adult male monkeys (Macaca fuscata fuscata, 8-9 kg). These animals had been used for other experiments carried out in our institute. Primary antibody (PAb) against telencephalin was obtained by immunizing mice with purified glycoprotein [11]. The procedures for immunostaining have been previously described in detail [8, 10, 11]. Briefly, 30/~m coronal sections were incubated with 0.03% Triton-X, then with 20% normal goat serum in PBS. Following several washes with PBS, sections were incubated for 2 h with polyclonal anti-telencephalin antiserum (1:100 dilution). Fluorescein isothiocyanate (FITC)-conjugated goat anti-mouse IgG was used as the second antibody. Neighboring sections were stained for cytochrome oxidase using Wong-Riley's protocol [13] or for Nissl substance with thionine. Fig. 1 compares anti-telencephalin antiserum (A),
119
IV V
Vl
I
II III
V VI
Fig. 1. lmmunofluorescence staining of the visual cortex with polyclonal antibody against telencephalin. A: a coronal section of the eat visual cortex (medial bank of the postlateral gyrus) was stained with the antibody. B: an adjacent section stained for cytochrome oxidase. C: thionine staining. D-F: corresponding sections from the monkey striate cortex. Lightly stained cytochrome oxidase blobs are indicated by arrows in E. Bar = 1 ram, Roman numerals, cortical layers. All of the regions shown are in area 17.
cytochrome oxidase (B) and Nissl staining (C) in the adult cat visual cortex. The white matter in the region of visual cortex was devoid of immunoreactivity to antitelencephalin antiserum (Fig. IA). In the gray matter, the antiserum faintly labeled layer IV, while intensely stained bundles of fibers were observed to perforate layer IV travelling toward the cortical surface. Cells of the other gray matter layers were intensely stained throughout except inside neuronal somata. In the section stained with cytochrome oxidase, a dense continuous band of high oxidative enzymatic activity was observed within layer IV (Fig. 1B). The neuropil within layers II, III and VI was moderately reactive. Layer V was distinguished for having a random distribution of highly reactive neurons against a rather light background. The expression of telencephalin is therefore significantly less pronounced in layer IV than in the other cortical layers, and in cat visual cortex it is complementary in distribution among the cortical layers to the expression of cytochrome oxidase. A similar relationship between the staining pattern for anti-telencephalin antiserum and
that for cytochrome oxidase was observed in monkey visual cortex (V1). The staining pattern achieved there with anti-telencephalin antiserum is shown in Fig. 1D. The white matter near the visual cortex was devoid of immunoreactivity, as was that of the cat. The immunoreactivity in layer IVa and IVc was quite low, although fine fiber processes in layer IVc were stained. The staining patterns in monkey V1 achieved with polyclonal anti-telencephalin antibody and with cytochrome oxidase were complementary, with the exception that immunofluorescence staining corresponding to cytochrome oxidase blobs was not found (Fig. 1D,E). Next, visual cortices of kittens of different ages were stained with polyclonal anti-telencephalin antibody in order to study postnatal developmental changes in staining (Fig. 2). In no brain examined was the white matter in the neighborhood of visual cortex labeled. In one week old kitten, immunoreactivity in the visual cortex was not pronounced, but blotchy regions of staining could be identified near the middle of the gray matter (Fig. 2A). A band of low immunoreactivity, possibly
120
Fig. 2. Developmentalchanges of immunofluorescencestaining of the cat visual cortex (medial bank of the postlateral gyrus, area 17) with antitelencephalinantibody. Coronal sectionswere obtained from postnatal 1-week-oldkitten (A), 3-week- (B), 5-week-(C), 7-week-(D), 9-week-(E), 13-week-(F), 17-week-old(G) and an adult (~3 years old) cat (H), respectively.Bar = 1 ram.
corresponding to that occurring in adult cortex, was observed also in the visual cortex of three week old kittens (Fig. 2B). Low immunoreactivity specific to layer IV was not clearly observable in the visual cortices of 5-, 7-, and 9-week-old kittens (Fig. 2C-E). Immunoreactivity in layer IV was relatively low in 9-week-old kitten (Fig. 2E) and was clearly lower there than in the other layers of the visual cortex of 13-week-old kitten (Fig. 2F). Low immunoreactivity in layer IV was also a conspicuous finding in 17-week-old kitten (Fig. 2G) and in adult cat (--~ 3 years old) (Fig. 2H). Previous studies have shown that telencephalin is expressed in the gray matter of all regions of the adult mammalian telencephalon, but not in non-telencephalic regions [10]. The present results demonstrate clearly that telencephalin expression varies by layer in the adult cat visual cortex. Specifically, immunoreactivity to telencephalin is considerably lower in layer IV than in other layers of the gray matter. Layers IVa and IVc in the monkey visual cortex also showed less immunoreactivity than other layers there. The diminished expression of telencephalin in layer IV was not specific to the visual
cortex but was observed also in several other regions of neocortex. This suggests that a basic pattern of telencephalin expression is common to all regions of the neocortex. Layer IV of the visual cortex receives massive inputs from thalamus. It has been shown in cat and monkey visual cortex that the termination sites of afferent fibers from the lateral geniculate nucleus correspond well to sites of dense cytochrome oxidase staining [6]. The present results have demonstrated that the sites of diminished expression of telencephalin coincide relatively well with those of intense cytochrome oxidase staining. This indicates that expression of telencephalin is decreased in those layers or sublayers in which massive thalamic afferent fibers terminate. These observations suggest that telencephalin expression on telencephalic neurons might be influenced by the massive afferent input from diencephalon. Observations relevant to the above have been made in the rabbit olfactory bulb [10]. In the adult bulb, expression of telencephalin has been shown to be diminished in the glomerular layer, in which olfactory nerve fibers
121 terminate massively on principal cells o f the bulb. Furthermore, a recent electron microscopic study has shown that telencephalin is not expressed by neurons which receive direct input f r o m olfactory nerve fibers (F. M u r a k a m i et al., personal communication). Considering these findings together with our own, it seems quite possible that the expression o f telencephalin is suppressed by massive direct afferents from non-telencephalic regions. The second m a j o r finding o f this study is that the expression o f telencephalin in cat visual cortex is developmentally regulated. It has already been reported that immunoreactivity against anti-telencephalin a n t i b o d y is barely detectable in m o s t regions o f the rabbit neocortex at birth, but increases during the early postnatal period [10]. In the present study, telencephalin has been shown to be present in all cortical layers o f cat visual cortex only between the age o f 4 to 13 weeks. Outside this time period, expression is substantially decreased in layer IV. The t e m p o r a l profile o f telencephalin expression in layer IV corresponds well to that o f the electrophysiologicallydefined sensitive period for visual cortical plasticity, including ocular d o m i n a n c e plasticity [7]. The results o f the present study suggest the intriguing possibility that the telencephalin m a y play a role in regulating ocular d o m i n a n c e plasticity. F u r t h e r studies will be necessary to test this hypothesis. We t h a n k Dr. M. C o n n o l l y for reading the m a n u s c r i p t and i m p r o v i n g the English. We also t h a n k Ms. N. M i k a jiri for secretarial service.
1 Blakemore, C., Maturation and modification in the developing visual system. In R. Held, H.W. Leibowitz and H.L. Teuber (Eds.), Handbook of Sensory Physiol., Vol. III, Springer, Berlin, 1978, pp. 377-436. 2 Dodd, J. and Jessell, T.M., Axon guidance and the patterning of neuron projections in vertebrates, Science, 242 (1988) 692-699. 3 Edelman, G.M., Cell adhesion molecules in the regulation of animal form and tissue pattern, Annu. Rev. Cell Biol., 2 (1986) 81116. 4 Frrgnac, Y. and Imbert, M., Development of neuronal selectivity in primary visual cortex of cat, Physiol. Rev., 64 (1984) 325-434. 5 Gilbert, C.D., Microcircuitry of the visual cortex, Annu. Rev. Neurosci., 6 (1983) 217-247. 6 Horton, J.C., Cytochrome oxidase patches: a new cytoarchitectonic feature of monkey visual cortex, Phil. Trans. R. Soc. Lond. Ser. B., 304 (1984) 199-253. 7 Hubel, D.H. and Wiesel, T.N., The period of susceptibility to the physiological effects of unilateral eye closure in kittens, J. Physiol., 206 (1970) 419-436. 8 Ikeda, J., Moil, K., Oka, S. and Watanabe, Y., A columnar arrangement of dendritic processes of entorhinal cortex neurons revealed by a monoclonal antibody, Brain Res., 505 (1989) 176179. 9 Kunemund, V., Jungalwala, F.B., Fisher, G., Cbou, D.K.H., Keilhauer, G. and Schachner, M., The L2/HNK-I carbohydrate of neural cell adhesion molecules is involved in cell interactions, J. Cell Biol., 106 (1988) 213-223. I0 Mori, K., Fujita, S.C., Watanabe, Y., Obata, K. and Hayaishi, O., Telencephalon-specific antigen identified by monoclonal antibody, Proc. Natl. Acad. Sci. U.S.A., 84 (1987) 3921-3925. 11 Oka, S., Moil, K. and Watanabe, Y., Mammalian telencephalic neurons express a segment-specific membrane glycoprotein, telencephalin, Neuroscience, 35 (1990) 93-103. 12 Pesheva, P., Horwitz, A.F. and Schachner, M., Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/ HNK-I and L3 carbohydrate structures shared by adhesion molecules, Neurosci. Lett., 83 (1987) 303-306. 13 Wong-Riley, M., Changes in the visual system of monocularly sutured or enucleated cat demonstrable with cytoehrome oxidase histochemistry, Brain Res., 171 (1979) 11-28.
