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Neuronal activity in primate visual cortex assessed by immunostaining for the transcription factor Zif268

Published online by Cambridge University Press:  02 June 2009

Avi Chaudhuri ,
Joanne A. Matsubara  and
Max S. Cynader
Avi Chaudhuri
Affiliation:
Department of Ophthalmology, University of British Columbia, Vancouver, British Columbia, Canada
Joanne A. Matsubara
Affiliation:
Department of Ophthalmology, University of British Columbia, Vancouver, British Columbia, Canada
Max S. Cynader
Affiliation:
Department of Ophthalmology, University of British Columbia, Vancouver, British Columbia, Canada
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Abstract

It is now well established that environmental signals mediated via neurotransmitters and hormones can induce responses in cells which involve a cascade of receptors, G proteins, and second messengers. These in turn can induce transcription factors which regulate long-term changes in gene expression. It has been proposed that the stimulus-transcription coupling properties of these DNA-binding proteins can be exploited to visualize activated neurons by way of immunostaining. We have used standard immunohistochemical techniques to detect the expression of one specific transcription factor, Zif268, in the visual cortex (area 17, V1) of vervet monkeys (Cercopithecus aethiops). Immunopositive neurons were present in large numbers throughout the visual cortex of the normal animal, being concentrated in layers 2/3 and 6 and at moderate levels in 4Cβ and 5. To determine if Zif268 expression was affected by visual stimulation in the monkey, we restricted light input to one eye with the aim of revealing ocular-dominance columns in striate cortex. We found that short-term monocular deprivation induced either by enucleation, intravitreal TTX injection, or eyelid suturing resulted in dramatic changes in Zif268 levels, revealing vertically oriented columns of reduced Zif268 staining interdigitated with columns of normal expression. Furthermore, these columns were discernible after just 2 h of monocular blockade. A comparison of the ocular-dominance pattern obtained with Zif268 immunostaining and cytochrome oxidase histochemistry in long-term monocularly deprived animals showed a coincident reduction of both markers along columns that were precisely aligned in adjacent sections, indicating that Zif268 expression is restricted to cortical regions of high metabolic activity. Simultaneous immunostaining for Zif268 and the calcium-binding proteins calbindin and parvalbumin showed a negative correlation, suggesting that the Zif268 protein may be expressed selectively within excitatory neurons. A similar approach with immunostaining for neurofilament and microtubule-associated proteins (SMI-32 and MAP2) revealed pyramidal neurons which were regularly found to contain a Zif268-positive nucleus. Furthermore, confocal images of lucifer yellow filled neurons possessing Zif268-positive nuclei all showed pyramidal morphology. Taken together, these results point to activity-dependent expression of Zif268 within a subset of excitatory neurons.

Keywords

Immediate-early geneFos-JunPlasticityArea 17Monkey
Type
Research Articles
Information
Visual Neuroscience , Volume 12 , Issue 1 , January 1995 , pp. 35 - 50
Copyright
Copyright © Cambridge University Press 1995

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References

Aronin, N., Sagar, S.M., Sharp, F.R. & Schwartz, W. (1990). Light regulates expression of a Fos-related protein in the rat SCN. Proceedings of the National Academy of Sciences of the U.S.A. 87, 5959–5962.CrossRefGoogle Scholar
Baimbridge, K.G. & Parkes, C.O. (1981). Vitamin D dependent calcium-binding in the chick brain. Cell Calcium 2, 65–77.CrossRefGoogle Scholar
Bartel, D.P., Sheng, M., Lau, L.F. & Greenberg, M.E. (1989). Growth factors and membrane depolarization activate distinct programs of early response gene expression: Dissociation of fos and jun induction. Genes and Development 3, 304–313.CrossRefGoogle ScholarPubMed
Blasdel, G.G. (1992). Differential imaging of ocular dominance and orientation selectivity in monkey striate cortex. Journal of Neuroscience 12, 3115–3138.Google Scholar
Blumcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1991). Parvalbumin in the monkey striate cortex: A quantitative immunoelectron-microscopy study. Brain Research 554, 237–243.Google Scholar
Blumcke, I., Hof, P.R., Morrison, J.H. & Celio, M.R. (1990). The distribution of parvalbumin in the visual cortex of Old World monkeys and humans. Journal of Comparative Neurology 301, 417–432.CrossRefGoogle ScholarPubMed
Born, R.T. & Tootell, R.B.H. (1991). Single-unit and 2-deoxyglucose studies of side inhibition in macaque striate cortex. Proceedings of the National Academy of Sciences of the U.S.A. 88, 7071–7075.CrossRefGoogle ScholarPubMed
Bravo, R., Burckhardt, J., Curran, T. & Muller, R. (1985). Stimulation and inhibition of growth by EOF in different A431 cell clones is accompanied by the rapid induction of c-fos and c-myc proto-oncogenes. European Molecular Biology Organization Journal 4, 1193–1197.Google Scholar
Bullttt, E. (1990). Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. Journal of Comparative Neurology 296, 517–530.CrossRefGoogle Scholar
Bullitt, E. (1989). Induction of c-fos-like protein within the lumbar spinal cord and thalamus of the rat following peripheral stimulation. Brain Research 493, 391–397.Google Scholar
Campbell, M.J. & Morrison, J.H. (1989). Monoclonal antibody to neu-rofilament protein (SMI-32) labels a subpopulation of pyramidal neurons in the human and monkey neocortex. Journal of Comparative Neurology 282, 191–205.Google Scholar
Carrol, W.M., Jennings, A.R. & Mastaglia, F.L. (1987). Reactive glial cells in CNS demyelination contain both GC and GFAP. Brain Research 411, 364–369.Google Scholar
Chaudhuri, A., Bravo, R., Liu, Y.L., Tidd, C., Matsubara, J.A. & Cynader, M.S. (1992 a). Ocular dominance columns in adult monkey revealed by immunocytochemical labelling for the transcription factor Krox-24 (NGF1-A). Investigative Ophthalmology and Visual Science (Suppl.) 33, 1131.Google Scholar
Chaudhuri, A., Dyck, R., Matsubara, J.A. & Cynader, M.S. (1992 b). Ocular dominance columns in monkey striate cortex revealed by activity-dependent expression of Zif268. Society for Neu-roscience Abstracts 18, 209.Google Scholar
Chaudhuri, A. & Cynader, M.S. (1993). Activity-dependent expression of the transcription factor Zif268 reveals ocular dominance columns in monkey striate cortex. Brain Research 605, 349–353.Google Scholar
Chaudhuri, A., Matsubara, J.A. & Cynader, M.S. (1993). Singlecell resolution of neuronal activity in the primate visual cortex: Labelling of excitatory neurons. Investigative Ophthalmology and Visual Science (Suppl.) 34, 793.Google Scholar
Christy, B.A., Lau, L.F. & Nathans, D. (1988). A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with “zinc finger” sequences. Proceedings of the National Academy of Sciences of the U.S.A. 85, 7857–7861.Google Scholar
Clark, M., Weiss, S.R.B. & Post, R.M. (1991). Expression of c-fos mRNA in rat brain after intracerebroventricular administration of corticotropin-releasing hormone. Neuroscience Letters 132, 235–238.CrossRefGoogle ScholarPubMed
Cole, A.J., Abu-Shakra, S., Saffen, D.W., Baraban, J.M. & Worley, P.F. (1990). Rapid rise in transcription factor mRNA's in rat brain after electroshock-induced seizures. Journal of Neurochemistry 55, 1920–1927.CrossRefGoogle ScholarPubMed
Cole, A.J., Saffen, D.W., Baraban, J.M. & Worley, P.F. (1989). Rapid increase of an immediate early gene messenger RNA in hip-pocampal neurons by synaptic NMDA receptor activation. Nature 340, 474–476.CrossRefGoogle Scholar
DeFelipe, J., Hendry, S.H.C. & Jones, E.G. (1989). Visualisation of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proceedings of the National Academy of Sciences of the U.S.A. 89, 2093–2097.Google Scholar
Dragunow, M. & Faull, R. (1989). The use of c-fos as a metabolic marker in neuronal pathway tracing. Journal of Neuroscience Methods 29, 261–265.Google Scholar
Dragunow, M. & Robertson, H.A. (1987). Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329, 441–442.Google Scholar
Duncan, G.E. & Stumpf, W.E. (1991). Brain activity patterns: Assessment by high resolution autoradiographic imaging of radiolabeled 2-deoxyglucose and glucose uptake. Progress in Neurobiology 37, 365–382.Google Scholar
Dyck, R.H., Chaudhuri, A. & Cynader, M.S. (1993). Zinc columns in primary visual cortex of adult vervet monkeys: Topographic distribution and effects of monocular impulse blockade. Society for Neuroscience Abstracts 19, 1799.Google Scholar
Earnest, D.J., Iadarola, M., Yeh, H.H. & Olschowka, J.A. (1990). Photic regulation of c-fos expression in neural components governing the entrainment of circadian rhythms. Experimental Neurology 109, 353–361.Google Scholar
Ehret, G. & Fischer, R. (1991). Neuronal activity and tonotopy in the auditory system visualized by c-fos gene expression. Brain Research 567, 350–354.Google Scholar
Florence, S.L. & Kaas, J.H. (1992). Ocular dominance columns in area 17 of Old World macaque and talapoin monkeys: Complete reconstructions and quantitative analyses. Visual Neuroscience 8, 449–462.Google Scholar
Friedman, H.R., Bruce, C.J. & Goldman-Rakic, P.S. (1989). Resolution of metabolic columns by a double-label 2-DG technique: Inter-digitation and coincidence in visual cortical areas of the same monkey. Journal of Neuroscience 9, 4111–4121.CrossRefGoogle Scholar
Fu, L. & Beckstead, R.M. (1992). Cortical stimulation induces fos expression in striatal neurons. Neuroscience 46, 329–334.CrossRefGoogle ScholarPubMed
Hendrickson, A.E. & Wilson, J.R. (1979). A difference in [14C] deoxyglucose autoradiographic patterns in striate cortex between Macaca and Saimiri monkeys following monocular stimulation. Brain Research 170, 353–358.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Bhandari, M.A. (1992). Neuronal organization and plasticity in adult monkey visual cortex: Immunoreactivity for micro-tubule associated protein 2. Visual Neuroscience 9, 445–459.Google Scholar
Hendry, S.H., Huntsman, M.M., Vinuela, A., Mohler, H., De Blas, A.L. & Jones, E.G. (1994). GABAA receptor subunit immunoreac-tivity in primate visual cortex: Distribution in macaques and humans and regulation by visual input in adulthood. Journal of Neuroscience 14, 2383–2401.CrossRefGoogle ScholarPubMed
Hendry, S.H.C. & Jones, E.G. (1988). Activity-dependent regulation of GAB A expression in the visual cortex of adult monkeys. Neuron 1, 701–712.Google Scholar
Hendry, S.H.C., Jones, E.G. & Burstein, N. (1988). Activity-dependent regulation of tachykinin-like immunoreactivity in neurons of monkey visual cortex. Journal of Neuroscience 8, 1225–1238.CrossRefGoogle ScholarPubMed
Hendry, S.H.C., Jones, E.G., Emson, P.C., Lawson, D.E.M., Heizmann, C.W. & Streit, P. (1989). Two classes of cortical GABA neurons defined by differential calcium binding protein immuno-reactivities. Experimental Brain Research 78, 467–472.Google Scholar
Hendry, S.H.C. & Kennedy, M.B. (1986). Immunoreactivity for a calmodulin-dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proceedings of the National Academy of Sciences of the U.S.A. 83, 1536–1540.Google Scholar
Herdegen, T., Leah, J.D., Zimmermann, M. & Bravo, R. (1990). The KROX-24 protein, a new transcription regulating factor: Expression in the rat central nervous system following afferent somato-sensory stimulation. Neuroscience Letters 120, 21–24.Google Scholar
Herdegen, T., Kummer, W., Fiallos, C.E., Leah, J. & Bravo, R. (1991). Expression of c-JUN, JUN B and JUN D proteins in rat nervous system following transection of vagus nerve and cervical sympathetic trunk. Neuroscience 45, 413–422.CrossRefGoogle Scholar
Hess, D.T. & Edwards, M.A. (1987). Anatomical demonstration of ocular segregation in the retinogeniculocortical pathway of the New World capuchin monkey (Cebus apelta). Journal of Comparative Neurology 264, 409–420.Google Scholar
Hevner, R.F. & Wong-Riley, M.T.T. (1990). Regulation of cytochrome oxidase protein levels by functional activity in the macaque monkey visual system. Journal of Neuroscience 10, 1331–1340.Google Scholar
Horton, J.C. & Hubel, D.H. (1981). Regular patchy distribution of cytochrome-oxidase staining in primary visual cortex of macaque monkey. Nature 292, 762–764.Google Scholar
Hubel, D.H. & Wiesel, T.N. (1972). Laminar and columnar distribution of genicul-cortical fibers in the macaque monkey. Journal of Comparative Neurology 146, 421–450.CrossRefGoogle ScholarPubMed
Hubel, D.H., Wiesel, T.N. & Stryker, M.P. (1978). Anatomical demonstration of orientation columns in macaque monkey. Journal of Comparative Neurology 177, 361–380.Google Scholar
Humphrey, A.L. & Hendrickson, A.E. (1983). Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey. Journal of Neuroscience 3, 345–358.Google Scholar
Huntsman, M.M., Isackson, P.J. & Jones, E.G. (1994). Lamina-specific expression and activity-dependent regulation of seven GABAA receptor subunit mRNAs in monkey visual cortex. Journal of Neuroscience 14, 2236–2259.CrossRefGoogle ScholarPubMed
Jones, K.J. & Evtnger, C. (1991). Differential neuronal expression of c-fos proto-oncogene following peripheral nerve injury or chemically-induced seizure. Journal of Neuroscience Research 28, 291–298.Google Scholar
Jorgenson, M., Deckert, J., Wright, D. & Gehlert, D. (1989). Delayed c-fos proto-oncogene expression in the rat hippocampus induced by transient global cerebral ischemia: An in situ hybridization study. Brain Research 484, 393–398.Google Scholar
Kennedy, C., Des Rosiers, M.H., Reivich, M., Sharps, F. & Sokoloff, L. (1975). Mapping of functional neural pathways by autoradiographic survey of local metabolic rate with [14C] deoxyglucose. Science 187, 850–853.Google Scholar
Kenndey, C., Des Rosiers, M.H., Sakurada, O., Shinohara, M., Rtevich, M., Jehle, J.W. & Sokoloff, L. (1976). Metabolic mapping of the primary visual system of the monkey by means of the autoradiographic [I4C] deoxyglucose technique. Proceedings of the National Academy of Sciences of the U.S.A. 73, 4230–4234.Google Scholar
Lau, L.F. & Nathans, D. (1987). Expression of a set of growth-related immediate-early genes in BALB/c 3T3 cells: Coordinate regulation with c-fos or c-myc. Proceedings of the National Academy of Sciences of the U.S.A. 84, 1182–1186.CrossRefGoogle ScholarPubMed
Leah, J.D., Herdegen, T. & Bravo, R. (1991). Selective expression of Jun proteins following axotomy and axonal transport block in peripheral nerves in the rat: Evidence for a role in the regeneration process. Brain Research 566, 198–207.Google Scholar
Lemaire, P., Relevant, O., Bravo, R. & Charnay, P. (1988). Two mouse genes encoding potential transcription factors with identical DNA-binding domains are activated by growth factors in cultured cells. Proceedings of the National Academy of Sciences of the U.S.A. 85, 4691–4695.Google Scholar
LeVay, S., Hubel, D.H. & Wiesel, T.N. (1975). The pattern of ocular dominance columns in macaque visual cortex revealed by a reduced silver stain. Journal of Comparative Neurology 159, 559–576.Google Scholar
Leventhal, A.G., Thompson, K.G., Liu, D., Neuman, L.M. & Ault, S.J. (1993). Form and color are not segregated in monkey striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 34, 813.Google Scholar
Lund, J.S. (1973). Organization of neurons in the visual cortex, area 17, of the monkey (Macaca mulatto). Journal of Comparative Neurology 147, 455–496.CrossRefGoogle Scholar
Lund, J.S. (1987). Local circuit neurons of macaque monkey striate cortex: I. Neurons of laminae 4c and 5a. Journal of Comparative Neurology 257, 60–92.Google Scholar
Milbrandt, J. (1986). Nerve growth factor rapidly induces c-fos mRNA in PC 12 rat pheochromocytoma cells. Proceedings of the National Academy of Sciences of the U.S.A. 83, 4789–4793.CrossRefGoogle Scholar
Milbrandt, J. (1987). A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science 238, 797–799.Google Scholar
Moratalla, R.., Robertson, H.A. & Graybiel, A.M. (1992). Dynamic regulation of NGFI-A (zif268, egrl) gene expression in the striatum. Journal of Neuroscience 12, 2609–2622.Google Scholar
O'Keefe, L.P., Levitt, J.B., Kiper, D.C., Shapley, R.M. & Movshon, J.A. (1993). Functional organization of owl monkey LGN and visual cortex. Investigative Ophthalmology and Visual Science (Suppl.) 34, 907.Google Scholar
Peters, A. & Sethares, C. (1991). Organization of pyramidal neurons in area 17 of monkey visual cortex. Journal of Comparative Neurology 306, 1–23.Google Scholar
Rea, M.A. (1989). Light increases fos-related protein immunoreactivity in the rat suprachiasmatic nuclei. Brain Research Bulletin 23, 577–581.Google Scholar
Rockland, K.S. & Virga, A. (1989). Terminal arbors of individual “feedback” axons projecting from area V2 to V1 in the macaque monkey: A study using immunohistochemistry of anterogradely transported Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology 285, 54–72.Google Scholar
Rosa, M.G.P., Gatass, R. & Fiorani, M. Jr., (1988). Complete pattern of ocular dominance stripes in V1 of a new world monkey, Cebus apella. Experimental Brain Research 72, 645–648.CrossRefGoogle ScholarPubMed
Sagar, S.M. & Sharp, F.R. (1990). Light induces a Fos-like nuclear antigen in retinal neurons. Molecular Brain Research 7, 17–21.CrossRefGoogle ScholarPubMed
Sagar, S.M., Sharp, F.R. & Curran, T. (1988). Expression of c-fos protein in brain: Metabolic mapping at the cellular level. Science 240, 1328–1331.CrossRefGoogle ScholarPubMed
Sandner, G., Di Scala, G., Rocha, B. & Angst, M.J. (1992). C-fos immunoreactivity in the brain following unilateral electrical stimulation of the dorsal periaqueductal gray in freely moving rats. Brain Research 573, 276–283.Google Scholar
Schwartz, E.L. & Rojer, A. (1992). A computational study of cortical hypercolumns and the topology of random orientation maps. Society for Neuroscience Abstracts 18, 742.Google Scholar
Seligman, A.M., Karnovsky, M.J., Wasserkrug, H.L. & Hanker, J.S. (1968). Non droplet ultrastructural demonstration of cytochrome oxidase activity with a polymerizing osmiophilic reagent, diamino-benzidine (DAB). Journal of Cell Biology 38, 1–14.CrossRefGoogle Scholar
Sharp, F.R., Griffith, J., Gonzalez, M.F. & Sagar, S.M. (1989 a). Trigeminal nerve section induces Fos-like immunoreactivity (FLI). in brainstem and decreases FLI in sensory cortex. Molecular Brain Research 6, 217–220.CrossRefGoogle ScholarPubMed
Sharp, F.R., Gonzalez, M.F., Sharp, J.W. & Sagar, S.M. (1989 b). c-fos expression and (14C)-2-deoxyglucose uptake in the caudal cerebellum of the rat during motor/sensory cortex stimulation. Journal of Comparative Neurology 284, 621–636.Google Scholar
Shin, C., McNamara, J.O., Morgan, J.I., Curran, T. & Cohen, D.R. (1990). Induction of c-fos mRNA expression by after-discharge in the hippocampus of naive and kindled rats. Journal of Neurochemistry 55, 1050–1055.CrossRefGoogle Scholar
Silverman, M.S. & Tootell, R.B.H. (1987). Modified technique for cytochrome oxidase histochemistry: Increased staining intensity and compatibility with 2-deoxyglucose autoradiography. Journal of Neuroscience Methods 19, 1–10.CrossRefGoogle ScholarPubMed
Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M.H., Patlak, C.S., Pettigrew, K.D., Sakurada, O. & Shinohara, M. (1977). The [14C]deoxyglucose method for measurement of local cerebral glucose utilization theory, procedure, and normal values in the conscious and anesthetized rat. Journal of Neurochemistry 28, 897–916.CrossRefGoogle Scholar
Sukhatme, V.P., Cao, X., Chang, L.C., Tsai-Morris, C.-H., Stamenkovich, D., Ferreira, P.C.P., Cohen, D.R., Edwards, S.A., Shows, T.B., Curran, T., Le Beau, M.M. & Adamson, E.D. (1988). A zinc finger-encoding gene coregulated with c-fos during growth and differentiation, and after cellular depolarization. Cell 53, 37–43.CrossRefGoogle ScholarPubMed
Teskey, G.C., Atkinson, B.G. & Cain, D.P. (1991). Expression of the proto-oncogene c-fos following electrical kindling in the rat. Molecular Brain Research 11, 1–10.CrossRefGoogle ScholarPubMed
Thejomayen, M.D. & Matsubara, J.A. (1993). Confocal microscopic study of the dendritic organization of patchy, intrinsic connections in area 18 of the cat. Cerebral Cortex 3, 442–453.Google Scholar
Tigges, M., Boothe, R.G., Tigges, J. & Wilson, J.R. (1992). Competition between an aphakic and an occluded eye for territory in striate cortex of developing rhesus monkeys: Cytochrome oxidase histochemistry in layer 4C. Journal of Comparative Neurology 316, 173–186.Google Scholar
Tootell, R.B.H., Silverman, M.S., Switkes, E. & DeValois, R.L. (1982)., Deoxyglucose analysis of retinotopic organization in primate striate cortex. Science 218, 902–904.CrossRefGoogle ScholarPubMed
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., DeValois, R.L. & Switkes, E. (1988 a). Functional anatomy of macaque striate cortex. I. Ocular dominance, binocular interactions, and baseline conditions. Journal of Neuroscience 8, 1500–1530.Google Scholar
Tootell, R.B.H., Switkes, E., Silverman, M.S. & Hamilton, S.L. (1988 b). Functional anatomy of macaque striate cortex. II. Retinotopic organization. Journal of Neuroscience 8, 1531–1568.Google Scholar
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., DeValois, R.L. & Switkes, E. (1988 c). Functional anatomy of macaque striate cortex. III. Color. Journal of Neuroscience 8, 1569–1593.Google Scholar
Tootell, R.B.H., Hamilton, S.L. & Switkes, E. (1988 d). Functional anatomy of macaque striate cortex. IV. Contrast and magno-parvo streams. Journal of Neuroscience 8, 1594–1609.Google Scholar
Tootell, R.B.H., Silverman, M.S., Hamilton, S.L., Swttkes, E. & DeValois, R.L. (1988 e). Functional anatomy of macaque striate cortex. V. Spatial frequency. Journal of Neuroscience 8, 1610–1624.Google Scholar
Ts'o, D.Y., Frostig, R.D., Lieke, E.E. & Grinvald, A. (1990). Functional organization of primate visual cortex revealed by high resolution optical imaging. Science 249, 417–420.Google Scholar
Ungerleider, L.G. & Desimone, R. (1986). Cortical connections of visual area MT in the macaque. Journal of Neurology 248, 190–222.Google Scholar
Van Brederode, J.F.M., Mulligan, K.A. & Hendrickson, A.E. (1990). Calcium-binding proteins as markers for subpopulations of GABAergic neurons in monkey striate cortex. Journal of Neurology 298, 1–22.Google Scholar
Wiesel, T.N., Hubel, D.H. & Lam, D.K.M. (1974). Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport. Brain Research 79, 273–279.Google Scholar
Williams, S., Evan, G.I. & Hunt, S.P. (1990). Changing patterns of c-fos induction in spinal neurons following thermal cutaneous stimulation in the rat. Neuroscience 36, 73–81.Google Scholar
Wong-Riley, M. & Carroll, E.W. (1984). Effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Nature 307, 262–264.Google Scholar
Wong-Riley, M.T.T., Tripathi, S.C., Trusk, T.C. & Hoppe, D.A. (1989 a). Effect of retinal impulse blockage on cytochrome oxidaserich zones in the macaque striate cortex: I. Quantitative electron-microscopic (EM) analysis of neurons. Visual Neuroscience 1, 483–497.Google Scholar
Wong-Riley, M.T.T., Trusk, T.C., Tripathi, S.C. & Hoppe, D.A. (1989 b). Effect of retinal impulse blockage on cytochrome oxidaserich zones in the macaque striate cortex: II. Quantitative electron-microscopic (EM) analysis of neuropil. Visual Neuroscience 2, 499–514.Google Scholar
Worley, P.F., Christy, B.A., Nakabeppu, Y., Bhat, R.V., Cole, A.J. & Baraban, J.M. (1991). Constitutive expression of zif268 in neocortex is regulated by synaptic activity. Proceedings of the National Academy of Sciences of the U.S.A. 88, 5106–5110.Google Scholar
Worley, P.F., Cole, A.J., Murphy, T.H., Christy, B.A., Nakabeppu, Y. & Baraban, J.M. (1990). Synaptic regulation of immediate-early genes in brain. Cold Spring Harbor Symposia on Quantitative Biology 55, 213–223.Google Scholar