0306-4522/92 $5.00 + 0.00 Pergamon Press Ltd ~i 1992 IBRO
Neuroscience Vol. 51, No. 4, pp. 749 753, 1992 Printed in Great Britain
Letter to Neuroscience P A R V A L B U M I N IMMUNOREACTIVITY: A RELIABLE M A R K E R FOR THE EFFECTS OF M O N O C U L A R DEPRIVATION IN THE RAT VISUAL CORTEX A. CELLERINO,* R. SICILIANO, L. DOMENICIand L. MAFFEI lstituto di Neurofisiologia del CNR, via S. Zeno 51, 56127 Pisa, and Scuola Normale Superiore, Pisa, Italy
In mammals, monocular deprivation performed during the early stages of postnatal development (critical period) dramatically affects the functional organization of the visual cortex. 1'6a2 Since the early work of Hubel and Wiesel, the effects of monocular deprivation are accounted for by the fibers driven by the two eyes competing for the control of cortical territories. In cat and monkey striking structural changes accompany the functional effects of monocular deprivation.7a4'15'21"23 Also, in the rat, monocular deprivation causes functional alteration at the level of visual cortex; 5''15" no structural correlates of these effects, however, have so far been described. Parvalbumin is a calcium binding protein that in the neocortex colocalizes with a subpopulation of GABAergic neurons.4z Here we report that in the rat monocular deprivation results in a dramatic reduction of parvalbumin-like immunoreactivity in the visual cortex contralateral to the deprived eye. This effect is due to competitive phenomena and not to visual deprivation itself, it is restricted to the binocular portion of the visual cortex and neither binocular deprivation, nor dark rearing can induce it. We conclude that parvalbumin-like immunoreactivity is a useful immunohistochemical marker for the effects of monocular deprivation in the rat visual cortex. Visual cortices of normal (n = 3) and monocularly deprived rats (n = 4) were reacted with parvalbumin antibodies. For normal rats the pattern of staining is shown in Fig. 1. Both cell bodies and terminal like dots are marked. The stained perikarya are uniformly distributed throughout all layers, with the exception of layer I: they are of various shapes and dimensions, most of them being medium-sized and fusiform. Several dendrite like processes are also stained (arrows Fig. lb). Stained terminals are pre-
*To whom correspondence should be addressed at: Istituto di Neurofisiologia del CNR. Abbreviation: LI, like immunoreactivity.
sent throughout layers II-VI with a denser band in layer V. Unstained cell bodies outlined by a rim of stained terminals can be noticed, in Fig. l b and c. The rat primary visual cortex can be subdivided into a monocular (OclM) and a binocular (OclB) subfields.2°~26 No gross differences of staining are evident between these two regions in normal animals (Fig. la). The pattern of parvalbumin-like immunoreactivity (LI) in MD rats is shown in Fig. 2 for the primary visual cortex contralateral to the deprived eye. In the monocular portion (area OclM) stained cell bodies, processes, terminals and unstained perikarya surrounded by terminals are present (Fig. 2a, b). By contrast, the binocular portion (area OclB) is void of stained neurons and processes. Terminal like dots are still present (Fig. 2a, c). In the binocular portion, several cells surrounded by a thick rim of heavily stained terminals can be found (Fig. 2c). They are medium-sized and poorly stained. In the cortex ipsilateral to the deprived eye the pattern of staining is not substantially modified with respect to normal animals (data not shown in figure). An explanation of this result could reside in the peculiar organization of the rat visual system. In this animal the great majority of the optic fibers do cross at the chiasm. Thus monocular deprivation could cause more massive functional rearrangements in the eontralateral cortex where the prominent input is depressed. This hypothesis is in accordance with results indicating that the unique anatomical effects described for the rat visual cortex, a reduction of the apical dendrite spines for the pyramidal cells of layer V, occurs only in the contralateral cortex, t7 Monocular deprivation performed after the end of the critical period ~7'~8(from P45 to P75, three rats) has no effect on parvalbumin-LI (data not shown in figure). Thus, in the rat visual cortex, parvalbumin is modulated by the visual input only during a restricted
749
750
A. CELLERINOel
al,
Fig. 1. Parvalbumin immunoreactivity in the visual cortex of normal rats. (a) Low-power microphotography. Monocular and binocular subfields are indicated as OclM and OclB, respectively. Arrowheads delineate the two subfields. Monocular and binocular subfields were identified on Nissb stained consecutive sections according to the atlas of Paxinos and Watson. '6 (b) Stained processes are indicated by arrowheads. (c) Unstained cell bodies outlined by immunopositive terminals are indicated by arrows. Scale bars = 500/~ m (a), 50/~ m (b), 10/~m (c). Perfusion: transcardially under choral hydrate anaesthesia (10.5 g/100 rot, 5 ml/kg), 200 ml 4% paraformaldehyde (Merck) in phosphate buffer pH 7.4, 0.1 M. Postfixation in the same fixative for 12 h at 4°C. Sectioning: Vibratome. 60 #m. Primary antibody: monoclonal anti-parvalbumin (Sigma) 1: 20,000, Triton X- 100 0.1%, normal goat serum 20% in phosphate-buffered saline 12h at 4~C. Secondary antibody: biotinylated goat anti-mouse affinity purified (Calbiochem) 1:1000, normal goat serum 5% in phosphate-buffered saline l h at room temperature under constant agitation. ABC kit (Vector Laboratories, Inc) 1 h at room temperature under constant agitation. Peroxidase was revealed by diaminobenzidine (0.05%) (Sigma) plus H202 (0.05%) and nickel ammonium sulphate (2.5%) (Carlo Erba, Italy) in acetate buffer 0.1 N, pH 6 a! room temperature.
time window that grossly corresponds to the critical period of the rat. We processed the visual cortices of dark-reared (n = 3) and binoculary deprived (n = 2) rats for parvaibumin-LI. Following these manipulations, classically used to test non-competitive effects induced by visual deprivation, parvalbumin-LI in the visual cortex is normal (Fig. 3). Our hypothesis is that parvalbumin-LI is regulated, during the critical period, by the competition between
the geniculate fibers driven by the two eyes for the control of the postsynaptic target. It is well known that monocular deprivation leads to a loss and/or suppression of the cortical synapses driven by the deprived eye and that this effect is present only in the binocular portion of the visual cortex. These changes in the connections could be reflected in a reduction of parvalbumin-LI. Another possibility could be that parvalbumin-LI is regulated by the crude electrical activity: This
Parvalbumin: a marker for monocular deprivation
751
Fig. 2. Parvalbumin-like immunoreactivity in the visual cortex contralateral to the deprived eye of monocularly deprived rats. (a) Low-power microphotography, monocular and binocular subfields are indicated as OclM and OclB, respectively. Arrowheads delineate these two areas. (b) Area OclM, tc) Area OcIB; high-power microphotography. In c loosely stained cells surrounded by a rim of stained terminals are indicated by arrowheads. Scale bars = 500pm (a), 25 ~m (b, c). Rats were deprived by means of eyelid suture under brief anaesthesia (diethylether) just before eye opening (postnatal day 14). At postnatal day 30 animals were killed and brain processed according to the protocol described in Fig. 1. possibility is very unlikely because neither binocular d e p r i v a t i o n n o r dark rearing has any effects u p o n parvalbumin-LI. We conclude that p a r v a l b u m i n - L I is a reliable m a r k e r for the effects of m o n o c u l a r d e p r i v a t i o n in the rat visual cortex. In recent years several i m m u n o - a n d histochemical m a r k e r s have been s h o w n to be regulated by visual experience in the cat a n d in the m o n k e y visual cortexg.8.9,~o 13.19,24,25 However, n o n e of them has been found to be strictly d e p e n d e n t u p o n b i n o c u l a r c o m p e t i t i o n as it is for p a r v a l b u m i n - L I in the rat visual cortex. It would be interesting to investigate whether p a r v a l b u m i n - L I also represents a specific
m a r k e r for the effects of m o n o c u l a r deprivation in other animal models. In the visual cortex of n o r m a l rats p a r v a l b u m i n co-localizes with a s u b p o p u l a t i o n of G A B A e r g i c neurons. It has been shown that in the adult m o n k e y visual cortex G A B A , its biosynthetic enzyme glutamate decarboxylase and other i m m u n o c h e m i c a l m a r k e r s related to the G A B A e r g i c circuitry are regulated by the visual input. 38'~° 13 It would be a point of interest to investigate whether in the rat the alteration of p a r v a l b u m i n - L I following m o n o c u l a r deprivation is due to a r e a r r a n g e m e n t of the G A B A e r g i c circuitry. Experiments are in progress to address this question.
REFERENCES
I. Baker F. M., Gripp P. and von Noorden G. K. (1974) Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in normal animals. Brain Res. 66, 185-208.
752
A. CELLER1NO et al.
Fig. 3. Parvalbumin-like immunoreactivity in the visual cortex of dark reared (a) and binocularly deprived (b) rats. Scale bars = 500/~m (a, b). Binocular deprivation: the rats were deprived by means of eyelid suture under brief anesthesia (diethylether) just before eye opening (postnatal day 14) and were killed at postnatal day 30. Dark rearing: animals were placed in a dark room together with the mother soon after birth and were reared in complete darkness until being killed (postnatal day 60). The protocol used for immunohistochemistry is described in Fig. 1.
2. Bear M. F., Schmechel D. E. and Ebner E. F. (1985) Glutamic acid decarboxylase in the striate cortex of normal and monocularly deprived kittens. J. Neurosci. 5, 1262-1275. 3. Benson D. L., Isackson P. J., Gall C. M. and Jones E. G. (1991) Differential effects of monocular deprivation on glutamic acid decarboxylase and type II calcium calmodulin dependent protein kinase gene expression in adult monkey visual cortex. J. Neurosci. 11, 3-47. 4. Celio M. R. (1986) Parvalbumin in most gamma amino butyric acid containing neurons in the rat cerebral cortex. Science 23, 995-997. 5. Celio M. R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 374-475. 5a. Domenici L., Bernardi N., Carmignoto G., Vantini G. and Maffei L. (1991) Nerve growth factor prevents the amblyopic effects of monocular deprivation. Proc. natn. Acad. Sci. U.S.A. ~ , 8811-8815. 6. Draeger U. (1978) Observation on monocular deprivation in mice. J. Neurophysiol. 41, 28-42. 7. Headon M. P. and Powell T. P. S. (1973) Cellular changes in the lateral geniculate nucleus of infant monkey after suture of the eyelids. J. Anat. 116, 135-145. 8. Hendry S. H. C. and Jones E. G. (1986) Reduction in the number of immunostained GABAergic neurons in deprived eye dominance columns of monkey area 17. Nature 320, 750-753. 9. Hendry S. H. C. and Kennedy M. B. (1986) Immunoreactivity for a calmodulin dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proc. natn. Acad. Sci. U.S.A. 83, 1536-1540. 10. Hendry S. H. C., Jones E. G., Hockfield S. and McKay R. D. G. (1988) Neuronal population stained with the monoclonal antibody Cat 301 in the mammalian cerebral cortex and thalamus. J, Neurosci. 8, 518-542. 11. Hendry S. H. C., Jones E. G. and Birestein N. (1988) Activity dependent regulation of tachykinin like immunoreactivity in neurons of monkey visual cortex. J. Neurosci. 8, 1225-1238. 12. Hendry S. H. C., Fuchs J., De Bias A. L. and Jones E. G. (1991) Distribution and plasticity ofimmunolocalized GABAa receptors in adult monkey visual cortex. J. Neurosci. 10, 2438-2450. 13. Horton J. C. and Hubel D. H. (1981) Regular patchy distribution of Cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762-764. 14. Hubel D. H., Wiesel T. N. and Le Vay S. (1977) Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. Soc. Lond. (Biol.) 278~ 377-409. 15. Le Vay S., Wiesel T. N. and Hubel D. H. (1980) The development of ocular dominance columns in normal and visually deprived monkeys. J. comp. Neurol. 191, t-51. 15a. Maffei L., Bernardi N., Domenici L., Parisi V. and Pizzorusso T. (1992) Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. J. Neurosci. (in press).
Parvalbumin: a marker for monocular deprivation
753
16. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Sydney. 17. Rothblatt L. A. and Schwartz M. L. (1979) The effect of monocular deprivation on dendritic spines in visual cortex of young and adult albino rats: evidences for a sensitive period. Brain Res. 161, 156-161. 18. Rothblatt L. A., Schwartz M. L. and Koschan P. M. (1978) Monocular deprivation in the rat: evidence for an age related deficit in visual behaviour. Brain Res. 158, 456-460. 19. Sandell J. H. (1986) NADPH diaphorase histochemistry in the Macaque striate cortex. J. comp, Neurol. 251,388-397. 20. Sefton A. J. and Dreher B. (1985) The visual system. In The Rat Nervous System (ed. Paxinos G.), Vol. I, pp. 169 210. Academic Press, Sydney. 21. Schatz C. J. and Stryker M. P. (1978) Ocular dominance in layer IV of the cat's visual cortex and the effects of visual deprivation. J. Physiol. 281, 267-283. 22. Wiesel T. N. and Hubel D. H. (1963) Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003 1007. 23. Wiesel T. N. and Hubel D. H. (1963) Effects of visual deprivation on morphology and physiology of cells in cat lateral geniculate body. J. NeurophysioL 26, 978-993. 24. Wong Riley M. T. T. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrated with cytochrome oxidase histochemistry. Brain Res. 171, 11 28. 25. Wong Riley M. T. T. (1984) Effect of impulse blockade on cytochrome oxidase activity in monkey visual system. Nature 307, 262 263. 26. Zilles K., Wree A., Schleicher A. and Divac I. (1984) The monocular binocular subfields of the rat's primary visual cortex: a quantitative morphological approach. J. comp. Neurol. 226, 391402. (Accepted 22 September 1992)
Neuroscience Vol. 51, No. 4, pp. 749 753, 1992 Printed in Great Britain
Letter to Neuroscience P A R V A L B U M I N IMMUNOREACTIVITY: A RELIABLE M A R K E R FOR THE EFFECTS OF M O N O C U L A R DEPRIVATION IN THE RAT VISUAL CORTEX A. CELLERINO,* R. SICILIANO, L. DOMENICIand L. MAFFEI lstituto di Neurofisiologia del CNR, via S. Zeno 51, 56127 Pisa, and Scuola Normale Superiore, Pisa, Italy
In mammals, monocular deprivation performed during the early stages of postnatal development (critical period) dramatically affects the functional organization of the visual cortex. 1'6a2 Since the early work of Hubel and Wiesel, the effects of monocular deprivation are accounted for by the fibers driven by the two eyes competing for the control of cortical territories. In cat and monkey striking structural changes accompany the functional effects of monocular deprivation.7a4'15'21"23 Also, in the rat, monocular deprivation causes functional alteration at the level of visual cortex; 5''15" no structural correlates of these effects, however, have so far been described. Parvalbumin is a calcium binding protein that in the neocortex colocalizes with a subpopulation of GABAergic neurons.4z Here we report that in the rat monocular deprivation results in a dramatic reduction of parvalbumin-like immunoreactivity in the visual cortex contralateral to the deprived eye. This effect is due to competitive phenomena and not to visual deprivation itself, it is restricted to the binocular portion of the visual cortex and neither binocular deprivation, nor dark rearing can induce it. We conclude that parvalbumin-like immunoreactivity is a useful immunohistochemical marker for the effects of monocular deprivation in the rat visual cortex. Visual cortices of normal (n = 3) and monocularly deprived rats (n = 4) were reacted with parvalbumin antibodies. For normal rats the pattern of staining is shown in Fig. 1. Both cell bodies and terminal like dots are marked. The stained perikarya are uniformly distributed throughout all layers, with the exception of layer I: they are of various shapes and dimensions, most of them being medium-sized and fusiform. Several dendrite like processes are also stained (arrows Fig. lb). Stained terminals are pre-
*To whom correspondence should be addressed at: Istituto di Neurofisiologia del CNR. Abbreviation: LI, like immunoreactivity.
sent throughout layers II-VI with a denser band in layer V. Unstained cell bodies outlined by a rim of stained terminals can be noticed, in Fig. l b and c. The rat primary visual cortex can be subdivided into a monocular (OclM) and a binocular (OclB) subfields.2°~26 No gross differences of staining are evident between these two regions in normal animals (Fig. la). The pattern of parvalbumin-like immunoreactivity (LI) in MD rats is shown in Fig. 2 for the primary visual cortex contralateral to the deprived eye. In the monocular portion (area OclM) stained cell bodies, processes, terminals and unstained perikarya surrounded by terminals are present (Fig. 2a, b). By contrast, the binocular portion (area OclB) is void of stained neurons and processes. Terminal like dots are still present (Fig. 2a, c). In the binocular portion, several cells surrounded by a thick rim of heavily stained terminals can be found (Fig. 2c). They are medium-sized and poorly stained. In the cortex ipsilateral to the deprived eye the pattern of staining is not substantially modified with respect to normal animals (data not shown in figure). An explanation of this result could reside in the peculiar organization of the rat visual system. In this animal the great majority of the optic fibers do cross at the chiasm. Thus monocular deprivation could cause more massive functional rearrangements in the eontralateral cortex where the prominent input is depressed. This hypothesis is in accordance with results indicating that the unique anatomical effects described for the rat visual cortex, a reduction of the apical dendrite spines for the pyramidal cells of layer V, occurs only in the contralateral cortex, t7 Monocular deprivation performed after the end of the critical period ~7'~8(from P45 to P75, three rats) has no effect on parvalbumin-LI (data not shown in figure). Thus, in the rat visual cortex, parvalbumin is modulated by the visual input only during a restricted
749
750
A. CELLERINOel
al,
Fig. 1. Parvalbumin immunoreactivity in the visual cortex of normal rats. (a) Low-power microphotography. Monocular and binocular subfields are indicated as OclM and OclB, respectively. Arrowheads delineate the two subfields. Monocular and binocular subfields were identified on Nissb stained consecutive sections according to the atlas of Paxinos and Watson. '6 (b) Stained processes are indicated by arrowheads. (c) Unstained cell bodies outlined by immunopositive terminals are indicated by arrows. Scale bars = 500/~ m (a), 50/~ m (b), 10/~m (c). Perfusion: transcardially under choral hydrate anaesthesia (10.5 g/100 rot, 5 ml/kg), 200 ml 4% paraformaldehyde (Merck) in phosphate buffer pH 7.4, 0.1 M. Postfixation in the same fixative for 12 h at 4°C. Sectioning: Vibratome. 60 #m. Primary antibody: monoclonal anti-parvalbumin (Sigma) 1: 20,000, Triton X- 100 0.1%, normal goat serum 20% in phosphate-buffered saline 12h at 4~C. Secondary antibody: biotinylated goat anti-mouse affinity purified (Calbiochem) 1:1000, normal goat serum 5% in phosphate-buffered saline l h at room temperature under constant agitation. ABC kit (Vector Laboratories, Inc) 1 h at room temperature under constant agitation. Peroxidase was revealed by diaminobenzidine (0.05%) (Sigma) plus H202 (0.05%) and nickel ammonium sulphate (2.5%) (Carlo Erba, Italy) in acetate buffer 0.1 N, pH 6 a! room temperature.
time window that grossly corresponds to the critical period of the rat. We processed the visual cortices of dark-reared (n = 3) and binoculary deprived (n = 2) rats for parvaibumin-LI. Following these manipulations, classically used to test non-competitive effects induced by visual deprivation, parvalbumin-LI in the visual cortex is normal (Fig. 3). Our hypothesis is that parvalbumin-LI is regulated, during the critical period, by the competition between
the geniculate fibers driven by the two eyes for the control of the postsynaptic target. It is well known that monocular deprivation leads to a loss and/or suppression of the cortical synapses driven by the deprived eye and that this effect is present only in the binocular portion of the visual cortex. These changes in the connections could be reflected in a reduction of parvalbumin-LI. Another possibility could be that parvalbumin-LI is regulated by the crude electrical activity: This
Parvalbumin: a marker for monocular deprivation
751
Fig. 2. Parvalbumin-like immunoreactivity in the visual cortex contralateral to the deprived eye of monocularly deprived rats. (a) Low-power microphotography, monocular and binocular subfields are indicated as OclM and OclB, respectively. Arrowheads delineate these two areas. (b) Area OclM, tc) Area OcIB; high-power microphotography. In c loosely stained cells surrounded by a rim of stained terminals are indicated by arrowheads. Scale bars = 500pm (a), 25 ~m (b, c). Rats were deprived by means of eyelid suture under brief anaesthesia (diethylether) just before eye opening (postnatal day 14). At postnatal day 30 animals were killed and brain processed according to the protocol described in Fig. 1. possibility is very unlikely because neither binocular d e p r i v a t i o n n o r dark rearing has any effects u p o n parvalbumin-LI. We conclude that p a r v a l b u m i n - L I is a reliable m a r k e r for the effects of m o n o c u l a r d e p r i v a t i o n in the rat visual cortex. In recent years several i m m u n o - a n d histochemical m a r k e r s have been s h o w n to be regulated by visual experience in the cat a n d in the m o n k e y visual cortexg.8.9,~o 13.19,24,25 However, n o n e of them has been found to be strictly d e p e n d e n t u p o n b i n o c u l a r c o m p e t i t i o n as it is for p a r v a l b u m i n - L I in the rat visual cortex. It would be interesting to investigate whether p a r v a l b u m i n - L I also represents a specific
m a r k e r for the effects of m o n o c u l a r deprivation in other animal models. In the visual cortex of n o r m a l rats p a r v a l b u m i n co-localizes with a s u b p o p u l a t i o n of G A B A e r g i c neurons. It has been shown that in the adult m o n k e y visual cortex G A B A , its biosynthetic enzyme glutamate decarboxylase and other i m m u n o c h e m i c a l m a r k e r s related to the G A B A e r g i c circuitry are regulated by the visual input. 38'~° 13 It would be a point of interest to investigate whether in the rat the alteration of p a r v a l b u m i n - L I following m o n o c u l a r deprivation is due to a r e a r r a n g e m e n t of the G A B A e r g i c circuitry. Experiments are in progress to address this question.
REFERENCES
I. Baker F. M., Gripp P. and von Noorden G. K. (1974) Effects of visual deprivation and strabismus on the response of neurons in the visual cortex of the monkey, including studies on the striate and prestriate cortex in normal animals. Brain Res. 66, 185-208.
752
A. CELLER1NO et al.
Fig. 3. Parvalbumin-like immunoreactivity in the visual cortex of dark reared (a) and binocularly deprived (b) rats. Scale bars = 500/~m (a, b). Binocular deprivation: the rats were deprived by means of eyelid suture under brief anesthesia (diethylether) just before eye opening (postnatal day 14) and were killed at postnatal day 30. Dark rearing: animals were placed in a dark room together with the mother soon after birth and were reared in complete darkness until being killed (postnatal day 60). The protocol used for immunohistochemistry is described in Fig. 1.
2. Bear M. F., Schmechel D. E. and Ebner E. F. (1985) Glutamic acid decarboxylase in the striate cortex of normal and monocularly deprived kittens. J. Neurosci. 5, 1262-1275. 3. Benson D. L., Isackson P. J., Gall C. M. and Jones E. G. (1991) Differential effects of monocular deprivation on glutamic acid decarboxylase and type II calcium calmodulin dependent protein kinase gene expression in adult monkey visual cortex. J. Neurosci. 11, 3-47. 4. Celio M. R. (1986) Parvalbumin in most gamma amino butyric acid containing neurons in the rat cerebral cortex. Science 23, 995-997. 5. Celio M. R. (1990) Calbindin D-28k and parvalbumin in the rat nervous system. Neuroscience 35, 374-475. 5a. Domenici L., Bernardi N., Carmignoto G., Vantini G. and Maffei L. (1991) Nerve growth factor prevents the amblyopic effects of monocular deprivation. Proc. natn. Acad. Sci. U.S.A. ~ , 8811-8815. 6. Draeger U. (1978) Observation on monocular deprivation in mice. J. Neurophysiol. 41, 28-42. 7. Headon M. P. and Powell T. P. S. (1973) Cellular changes in the lateral geniculate nucleus of infant monkey after suture of the eyelids. J. Anat. 116, 135-145. 8. Hendry S. H. C. and Jones E. G. (1986) Reduction in the number of immunostained GABAergic neurons in deprived eye dominance columns of monkey area 17. Nature 320, 750-753. 9. Hendry S. H. C. and Kennedy M. B. (1986) Immunoreactivity for a calmodulin dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proc. natn. Acad. Sci. U.S.A. 83, 1536-1540. 10. Hendry S. H. C., Jones E. G., Hockfield S. and McKay R. D. G. (1988) Neuronal population stained with the monoclonal antibody Cat 301 in the mammalian cerebral cortex and thalamus. J, Neurosci. 8, 518-542. 11. Hendry S. H. C., Jones E. G. and Birestein N. (1988) Activity dependent regulation of tachykinin like immunoreactivity in neurons of monkey visual cortex. J. Neurosci. 8, 1225-1238. 12. Hendry S. H. C., Fuchs J., De Bias A. L. and Jones E. G. (1991) Distribution and plasticity ofimmunolocalized GABAa receptors in adult monkey visual cortex. J. Neurosci. 10, 2438-2450. 13. Horton J. C. and Hubel D. H. (1981) Regular patchy distribution of Cytochrome oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762-764. 14. Hubel D. H., Wiesel T. N. and Le Vay S. (1977) Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. Soc. Lond. (Biol.) 278~ 377-409. 15. Le Vay S., Wiesel T. N. and Hubel D. H. (1980) The development of ocular dominance columns in normal and visually deprived monkeys. J. comp. Neurol. 191, t-51. 15a. Maffei L., Bernardi N., Domenici L., Parisi V. and Pizzorusso T. (1992) Nerve growth factor (NGF) prevents the shift in ocular dominance distribution of visual cortical neurons in monocularly deprived rats. J. Neurosci. (in press).
Parvalbumin: a marker for monocular deprivation
753
16. Paxinos G. and Watson C. (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Sydney. 17. Rothblatt L. A. and Schwartz M. L. (1979) The effect of monocular deprivation on dendritic spines in visual cortex of young and adult albino rats: evidences for a sensitive period. Brain Res. 161, 156-161. 18. Rothblatt L. A., Schwartz M. L. and Koschan P. M. (1978) Monocular deprivation in the rat: evidence for an age related deficit in visual behaviour. Brain Res. 158, 456-460. 19. Sandell J. H. (1986) NADPH diaphorase histochemistry in the Macaque striate cortex. J. comp, Neurol. 251,388-397. 20. Sefton A. J. and Dreher B. (1985) The visual system. In The Rat Nervous System (ed. Paxinos G.), Vol. I, pp. 169 210. Academic Press, Sydney. 21. Schatz C. J. and Stryker M. P. (1978) Ocular dominance in layer IV of the cat's visual cortex and the effects of visual deprivation. J. Physiol. 281, 267-283. 22. Wiesel T. N. and Hubel D. H. (1963) Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol. 26, 1003 1007. 23. Wiesel T. N. and Hubel D. H. (1963) Effects of visual deprivation on morphology and physiology of cells in cat lateral geniculate body. J. NeurophysioL 26, 978-993. 24. Wong Riley M. T. T. (1979) Changes in the visual system of monocularly sutured or enucleated cats demonstrated with cytochrome oxidase histochemistry. Brain Res. 171, 11 28. 25. Wong Riley M. T. T. (1984) Effect of impulse blockade on cytochrome oxidase activity in monkey visual system. Nature 307, 262 263. 26. Zilles K., Wree A., Schleicher A. and Divac I. (1984) The monocular binocular subfields of the rat's primary visual cortex: a quantitative morphological approach. J. comp. Neurol. 226, 391402. (Accepted 22 September 1992)
