Abstract
A theory is proposed that biochemical changes at the synapse that occur as a result of stimulation of specific neuronal circuits can lead to long-term changes only if alterations occur in synaptic structures in these circuits. The main synaptic structure that is thought to undergo this alteration is the postsynaptic density (PSD). There are many reports in the literature of overall structural changes at the synapse, including the PSD, resulting from various neuronal stimuli. These structural changes are here envisaged to include those of concentration and conformation of PSD proteins, changes that could alter the neural physiology of dendritic spines and even that of the presynaptic terminal.
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Selected References
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- Ackerman S. K., Zur Nedden D., Heintzelman M., Hunkapiller M., Zoon K. Biologic activity in a fragment of recombinant human interferon alpha. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1045–1047. doi: 10.1073/pnas.81.4.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berard D. R., Burgess J. W., Coss R. G. Plasticity of dendritic spine formation: a state-dependent stochastic process. Int J Neurosci. 1981;13(2-3):93–98. doi: 10.3109/00207458109043306. [DOI] [PubMed] [Google Scholar]
- Blomberg F., Cohen R. S., Siekevitz P. The structure of postsynaptic densities isolated from dog cerebral cortex. II. Characterization and arrangement of some of the major proteins within the structure. J Cell Biol. 1977 Jul;74(1):204–225. doi: 10.1083/jcb.74.1.204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bloom F. E., Ueda T., Battenberg E., Greengard P. Immunocytochemical localization, in synapses, of protein I, an endogenous substrate for protein kinases in mammalian brain. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5982–5986. doi: 10.1073/pnas.76.11.5982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brandon J. G., Coss R. G. Rapid dendritic spine stem shortening during one-trial learning: the honeybee's first orientation flight. Brain Res. 1982 Dec 2;252(1):51–61. doi: 10.1016/0006-8993(82)90977-5. [DOI] [PubMed] [Google Scholar]
- Bär P. R., Schotman P., Gispen W. H., Tielen A. M., Lopes Da Silva F. H. Changes in synaptic membrane phosphorylation after tetanic stimulation in the dentate area of the rat hippocampal slice. Brain Res. 1980 Oct 6;198(2):478–484. doi: 10.1016/0006-8993(80)90764-7. [DOI] [PubMed] [Google Scholar]
- Carlin R. K., Grab D. J., Cohen R. S., Siekevitz P. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol. 1980 Sep;86(3):831–845. doi: 10.1083/jcb.86.3.831. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlin R. K., Grab D. J., Siekevitz P. Function of a calmodulin in postsynaptic densities. III. Calmodulin-binding proteins of the postsynaptic density. J Cell Biol. 1981 Jun;89(3):449–455. doi: 10.1083/jcb.89.3.449. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carlin R. K., Grab D. J., Siekevitz P. Postmortem accumulation of tubulin in postsynaptic density preparations. J Neurochem. 1982 Jan;38(1):94–100. doi: 10.1111/j.1471-4159.1982.tb10858.x. [DOI] [PubMed] [Google Scholar]
- Carlin R. K., Siekevitz P. Characterization of Na+-independent GABA and flunitrazepam binding sites in preparations of synaptic membranes and postsynaptic densities isolated from canine cerebral cortex and cerebellum. J Neurochem. 1984 Oct;43(4):1011–1017. doi: 10.1111/j.1471-4159.1984.tb12837.x. [DOI] [PubMed] [Google Scholar]
- Carlin R. K., Siekevitz P. Plasticity in the central nervous system: do synapses divide? Proc Natl Acad Sci U S A. 1983 Jun;80(11):3517–3521. doi: 10.1073/pnas.80.11.3517. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen R. S., Blomberg F., Berzins K., Siekevitz P. The structure of postsynaptic densities isolated from dog cerebral cortex. I. Overall morphology and protein composition. J Cell Biol. 1977 Jul;74(1):181–203. doi: 10.1083/jcb.74.1.181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen R. S., Carlin R. K., Grab D. J., Siekevitz P. Phosphoproteins in postsynaptic densities. Prog Brain Res. 1982;56:49–76. doi: 10.1016/S0079-6123(08)63768-1. [DOI] [PubMed] [Google Scholar]
- Cohen R. S., Siekevitz P. Form of the postsynaptic density. A serial section study. J Cell Biol. 1978 Jul;78(1):36–46. doi: 10.1083/jcb.78.1.36. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cohen R. S., Wolosewick J. J., Becker R. P., Pappas G. D. Fine structure of synapses of the central nervous system in resinless sections. J Submicrosc Cytol. 1983 Oct;15(4):849–863. [PubMed] [Google Scholar]
- Coss R. G., Globus A. Social experience affects the development of dendritic spines and branches on tectal interneurons in the jewel fish. Dev Psychobiol. 1979 Jul;12(4):347–358. doi: 10.1002/dev.420120409. [DOI] [PubMed] [Google Scholar]
- Coss R. G., Globus A. Spine stems on tectal interneurons in jewel fish are shortened by social stimulation. Science. 1978 May 19;200(4343):787–790. doi: 10.1126/science.644322. [DOI] [PubMed] [Google Scholar]
- Crick F. Memory and molecular turnover. Nature. 1984 Nov 8;312(5990):101–101. doi: 10.1038/312101a0. [DOI] [PubMed] [Google Scholar]
- Davis J. Q., Bennett V. Brain ankyrin. A membrane-associated protein with binding sites for spectrin, tubulin, and the cytoplasmic domain of the erythrocyte anion channel. J Biol Chem. 1984 Nov 10;259(21):13550–13559. [PubMed] [Google Scholar]
- De Blas A. L., Wang Y. J., Sorensen R., Mahler H. R. Protein phosphorylation in synaptic membranes regulated by adenosine 3':5'-monophosphate: regional and subcellular distribution of the endogenous substrates. J Neurochem. 1979 Sep;33(3):647–659. doi: 10.1111/j.1471-4159.1979.tb05209.x. [DOI] [PubMed] [Google Scholar]
- De Camilli P., Harris S. M., Jr, Huttner W. B., Greengard P. Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes. J Cell Biol. 1983 May;96(5):1355–1373. doi: 10.1083/jcb.96.5.1355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Desmond N. L., Levy W. B. Synaptic correlates of associative potentiation/depression: an ultrastructural study in the hippocampus. Brain Res. 1983 Apr 11;265(1):21–30. doi: 10.1016/0006-8993(83)91329-x. [DOI] [PubMed] [Google Scholar]
- Duffy C., Teyler T. J., Shashoua V. E. Long-term potentiation in the hippocampal slice: evidence for stimulated secretion of newly synthesized proteins. Science. 1981 Jun 5;212(4499):1148–1151. doi: 10.1126/science.7233208. [DOI] [PubMed] [Google Scholar]
- Dyson S. E., Jones D. G. Synaptic remodelling during development and maturation: junction differentiation and splitting as a mechanism for modifying connectivity. Brain Res. 1984 Mar;315(1):125–137. doi: 10.1016/0165-3806(84)90084-1. [DOI] [PubMed] [Google Scholar]
- Fagg G. E., Matus A. Selective association of N-methyl aspartate and quisqualate types of L-glutamate receptor with brain postsynaptic densities. Proc Natl Acad Sci U S A. 1984 Nov;81(21):6876–6880. doi: 10.1073/pnas.81.21.6876. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feit H., Kelly P., Cotman C. W. Identification of a protein related to tubulin in the postsynaptic density. Proc Natl Acad Sci U S A. 1977 Mar;74(3):1047–1051. doi: 10.1073/pnas.74.3.1047. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fifková E., Anderson C. L., Young S. J., Van Harreveld A. Effect of anisomycin on stimulation-induced changes in dendritic spines of the dentate granule cells. J Neurocytol. 1982 Apr;11(2):183–210. doi: 10.1007/BF01258243. [DOI] [PubMed] [Google Scholar]
- Fifková E., Delay R. J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol. 1982 Oct;95(1):345–350. doi: 10.1083/jcb.95.1.345. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fifková E., Van Harreveld A. Long-lasting morphological changes in dendritic spines of dentate granular cells following stimulation of the entorhinal area. J Neurocytol. 1977 Apr;6(2):211–230. doi: 10.1007/BF01261506. [DOI] [PubMed] [Google Scholar]
- Goldenring J. R., McGuire J. S., Jr, DeLorenzo R. J. Identification of the major postsynaptic density protein as homologous with the major calmodulin-binding subunit of a calmodulin-dependent protein kinase. J Neurochem. 1984 Apr;42(4):1077–1084. doi: 10.1111/j.1471-4159.1984.tb12713.x. [DOI] [PubMed] [Google Scholar]
- Grab D. J., Berzins K., Cohen R. S., Siekevitz P. Presence of calmodulin in postsynaptic densities isolated from canine cerebral cortex. J Biol Chem. 1979 Sep 10;254(17):8690–8696. [PubMed] [Google Scholar]
- Grab D. J., Carlin R. K., Siekevitz P. Function of a calmodulin in postsynaptic densities. II. Presence of a calmodulin-activatable protein kinase activity. J Cell Biol. 1981 Jun;89(3):440–448. doi: 10.1083/jcb.89.3.440. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grab D. J., Carlin R. K., Siekevitz P. Function of calmodulin in postsynaptic densities. I. Presence of a calmodulin-activatable cyclic nucleotide phosphodiesterase activity. J Cell Biol. 1981 Jun;89(3):433–439. doi: 10.1083/jcb.89.3.433. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greenough W. T., West R. W., DeVoogd T. J. Subsynaptic plate perforations: changes with age and experience in the rat. Science. 1978 Dec 8;202(4372):1096–1098. doi: 10.1126/science.715459. [DOI] [PubMed] [Google Scholar]
- Groswald D. E., Kelly P. T. Evidence that a cerebellum-enriched, synaptic junction glycoprotein is related to fodrin and resists extraction with triton in a calcium-dependent manner. J Neurochem. 1984 Feb;42(2):534–546. doi: 10.1111/j.1471-4159.1984.tb02711.x. [DOI] [PubMed] [Google Scholar]
- Gulley R. L., Reese T. S. Cytoskeletal organization at the postsynaptic complex. J Cell Biol. 1981 Oct;91(1):298–302. doi: 10.1083/jcb.91.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gurd J. W. Identification of lectin receptors associated with rat brain postsynaptic densities. Brain Res. 1977 Apr 22;126(1):154–159. doi: 10.1016/0006-8993(77)90222-0. [DOI] [PubMed] [Google Scholar]
- Güldner F. H., Ingham C. A. Increase in postsynaptic density material in optic target neurons of the rat suprachiasmatic nucleus after bilateral enucleation. Neurosci Lett. 1980 Apr;17(1-2):27–31. doi: 10.1016/0304-3940(80)90056-7. [DOI] [PubMed] [Google Scholar]
- Güldner F. H., Ingham C. A. Plasticity in synaptic appositions of optic nerve afferents under different lighting conditions. Neurosci Lett. 1979 Oct;14(2-3):235–240. doi: 10.1016/0304-3940(79)96154-8. [DOI] [PubMed] [Google Scholar]
- Harreveld A. V., Trubatch J. Synaptic changes in frog brain after stimulation with potassium chloride. J Neurocytol. 1975 Feb;4(1):33–46. doi: 10.1007/BF01099093. [DOI] [PubMed] [Google Scholar]
- Illis L. S. Enlargement of spinal cord synapses after repetitive stimulation of a single posterior root. Nature. 1969 Jul 5;223(5201):76–77. doi: 10.1038/223076a0. [DOI] [PubMed] [Google Scholar]
- Jonec V., Walsterlain C. G. Effect of inhibitors of protein synthesis on the development of kindled seizures in rats. Exp Neurol. 1979 Dec;66(3):524–532. doi: 10.1016/0014-4886(79)90199-7. [DOI] [PubMed] [Google Scholar]
- Kalichman M. W., Burnham W. M., Livingston K. E. Pharmacological investigation of gamma-aminobutyric acid (GABA) and fully-developed generalized seizures in the amygdala-kindled rat. Neuropharmacology. 1982 Feb;21(2):127–131. doi: 10.1016/0028-3908(82)90151-4. [DOI] [PubMed] [Google Scholar]
- Kalichman M. W. Neurochemical correlates of the kindling model of epilepsy. Neurosci Biobehav Rev. 1982 Summer;6(2):165–181. doi: 10.1016/0149-7634(82)90053-7. [DOI] [PubMed] [Google Scholar]
- Kelly P. T., Cotman C. W. Identification of glycoproteins and proteins at synapses in the central nervous system. J Biol Chem. 1977 Jan 25;252(2):786–793. [PubMed] [Google Scholar]
- Kelly P. T., Cotman C. W., Largen M. Cyclic AMP-stimulated protein kinases at brain synaptic junctions. J Biol Chem. 1979 Mar 10;254(5):1564–1575. [PubMed] [Google Scholar]
- Kelly P. T., Cotman C. W. Synaptic proteins. Characterization of tubulin and actin and identification of a distinct postsynaptic density polypeptide. J Cell Biol. 1978 Oct;79(1):173–183. doi: 10.1083/jcb.79.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kelly P. T., Cotman C. W. Synaptic proteins. Characterization of tubulin and actin and identification of a distinct postsynaptic density polypeptide. J Cell Biol. 1978 Oct;79(1):173–183. doi: 10.1083/jcb.79.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kennedy M. B., Bennett M. K., Erondu N. E. Biochemical and immunochemical evidence that the "major postsynaptic density protein" is a subunit of a calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A. 1983 Dec;80(23):7357–7361. doi: 10.1073/pnas.80.23.7357. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kennedy M. B. Experimental approaches to understanding the role of protein phosphorylation in the regulation of neuronal function. Annu Rev Neurosci. 1983;6:493–525. doi: 10.1146/annurev.ne.06.030183.002425. [DOI] [PubMed] [Google Scholar]
- Lee K. S., Schottler F., Oliver M., Lynch G. Brief bursts of high-frequency stimulation produce two types of structural change in rat hippocampus. J Neurophysiol. 1980 Aug;44(2):247–258. doi: 10.1152/jn.1980.44.2.247. [DOI] [PubMed] [Google Scholar]
- Lester B. R., Miller A. L., Peck E. J., Jr Differential solubilization of gamma-aminobutyric acid receptive sites from membranes of mammalian brain. J Neurochem. 1981 Jan;36(1):154–164. doi: 10.1111/j.1471-4159.1981.tb02390.x. [DOI] [PubMed] [Google Scholar]
- Levine J., Willard M. Fodrin: axonally transported polypeptides associated with the internal periphery of many cells. J Cell Biol. 1981 Sep;90(3):631–642. doi: 10.1083/jcb.90.3.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lin C. T., Dedman J. R., Brinkley B. R., Means A. R. Localization of calmodulin in rat cerebellum by immunoelectron microscopy. J Cell Biol. 1980 May;85(2):473–480. doi: 10.1083/jcb.85.2.473. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch G., Baudry M. The biochemistry of memory: a new and specific hypothesis. Science. 1984 Jun 8;224(4653):1057–1063. doi: 10.1126/science.6144182. [DOI] [PubMed] [Google Scholar]
- Manina A. A. The synapses of the nervous system. Int Rev Cytol. 1979;57:345–383. doi: 10.1016/s0074-7696(08)61466-7. [DOI] [PubMed] [Google Scholar]
- Matus A. I., Taff-Jones D. H. Morphology and molecular composition of isolated postsynaptic junctional structures. Proc R Soc Lond B Biol Sci. 1978 Dec 4;203(1151):135–151. doi: 10.1098/rspb.1978.0097. [DOI] [PubMed] [Google Scholar]
- Matus A., Pehling G., Wilkinson D. gamma-Aminobutyric acid receptors in brain postsynaptic densities. J Neurobiol. 1981 Jan;12(1):67–73. doi: 10.1002/neu.480120106. [DOI] [PubMed] [Google Scholar]
- McNamara J. O., Byrne M. C., Dasheiff R. M., Fitz J. G. The kindling model of epilepsy: a review. Prog Neurobiol. 1980;15(2):139–159. doi: 10.1016/0301-0082(80)90006-4. [DOI] [PubMed] [Google Scholar]
- McNamara J. O. Role of neurotransmitters in seizure mechanisms in the kindling model of epilepsy. Fed Proc. 1984 Jul;43(10):2516–2520. [PubMed] [Google Scholar]
- Mollgaard K., Diamond M. C., Bennett E. L., Rosenzweig M. R., Lindner B. Quantitative synaptic changes with differential experience in rat brain. Int J Neurosci. 1971 Sep;2(3):113–127. doi: 10.3109/00207457109148764. [DOI] [PubMed] [Google Scholar]
- Nieto-Sampedro M., Hoff S. F., Cotman C. W. Perforated postsynaptic densities: probable intermediates in synapse turnover. Proc Natl Acad Sci U S A. 1982 Sep;79(18):5718–5722. doi: 10.1073/pnas.79.18.5718. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peters A., Kaiserman-Abramof I. R. The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Z Zellforsch Mikrosk Anat. 1969 Sep 22;100(4):487–506. doi: 10.1007/BF00344370. [DOI] [PubMed] [Google Scholar]
- Peterson D. W., Collins J. F., Bradford H. F. Anticonvulsant action of amino acid antagonists against kindled hippocampal seizures. Brain Res. 1984 Oct 8;311(1):176–180. doi: 10.1016/0006-8993(84)91414-8. [DOI] [PubMed] [Google Scholar]
- Peterson D. W., Collins J. F., Bradford H. F. The kindled amygdala model of epilepsy: anticonvulsant action of amino acid antagonists. Brain Res. 1983 Sep 19;275(1):169–172. doi: 10.1016/0006-8993(83)90431-6. [DOI] [PubMed] [Google Scholar]
- Peterson S. L., Albertson T. E. Neurotransmitter and neuromodulator function in the kindled seizure and state. Prog Neurobiol. 1982;19(4):237–270. doi: 10.1016/0301-0082(82)90008-9. [DOI] [PubMed] [Google Scholar]
- RICHTER D. FACTORS INFLUENCING THE PROTEIN METABOLISM OF THE BRAIN. Br Med Bull. 1965 Jan;21:76–80. doi: 10.1093/oxfordjournals.bmb.a070361. [DOI] [PubMed] [Google Scholar]
- Rostas J. A., Kelly P. T., Pesin R. H., Cotman C. W. Protein and glycoprotein composition of synaptic junctions prepared from discrete synaptic regions and different species. Brain Res. 1979 May 18;168(1):151–167. doi: 10.1016/0006-8993(79)90133-1. [DOI] [PubMed] [Google Scholar]
- Rutledge L. T., Wright C., Duncan J. Morphological changes in pyramidal cells of mammalian neocortex associated with increased use. Exp Neurol. 1974 Aug;44(2):209–228. doi: 10.1016/0014-4886(74)90060-0. [DOI] [PubMed] [Google Scholar]
- Siekevitz P. Biological membranes: the dynamics of their organization. Annu Rev Physiol. 1972;34:117–140. doi: 10.1146/annurev.ph.34.030172.001001. [DOI] [PubMed] [Google Scholar]
- Steward O. Alterations in polyribosomes associated with dendritic spines during the reinnervation of the dentate gyrus of the adult rat. J Neurosci. 1983 Jan;3(1):177–188. doi: 10.1523/JNEUROSCI.03-01-00177.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steward O., Levy W. B. Preferential localization of polyribosomes under the base of dendritic spines in granule cells of the dentate gyrus. J Neurosci. 1982 Mar;2(3):284–291. doi: 10.1523/JNEUROSCI.02-03-00284.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steward O. Polyribosomes at the base of dendritic spines of central nervous system neurons--their possible role in synapse construction and modification. Cold Spring Harb Symp Quant Biol. 1983;48(Pt 2):745–759. doi: 10.1101/sqb.1983.048.01.077. [DOI] [PubMed] [Google Scholar]
- Strader C. D., Pickel V. M., Joh T. H., Strohsacker M. W., Shorr R. G., Lefkowitz R. J., Caron M. G. Antibodies to the beta-adrenergic receptor: attenuation of catecholamine-sensitive adenylate cyclase and demonstration of postsynaptic receptor localization in brain. Proc Natl Acad Sci U S A. 1983 Apr;80(7):1840–1844. doi: 10.1073/pnas.80.7.1840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tilney L. G., Detmers P. Actin in erythrocyte ghosts and its association with spectrin. Evidence for a nonfilamentous form of these two molecules in situ. J Cell Biol. 1975 Sep;66(3):508–520. doi: 10.1083/jcb.66.3.508. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tuff L. P., Racine R. J., Adamec R. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. I. Paired-pulse depression. Brain Res. 1983 Oct 24;277(1):79–90. doi: 10.1016/0006-8993(83)90909-5. [DOI] [PubMed] [Google Scholar]
- Tuff L. P., Racine R. J., Mishra R. K. The effects of kindling on GABA-mediated inhibition in the dentate gyrus of the rat. II. Receptor binding. Brain Res. 1983 Oct 24;277(1):91–98. doi: 10.1016/0006-8993(83)90910-1. [DOI] [PubMed] [Google Scholar]
- Ueda T., Greengard P., Berzins K., Cohen R. S., Blomberg F., Grab D. J., Siekevitz P. Subcellular distribution in cerebral cortex of two proteins phosphorylated by a cAMP-dependent protein kinase. J Cell Biol. 1979 Nov;83(2 Pt 1):308–319. doi: 10.1083/jcb.83.2.308. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uylings H. B., Kuypers K., Diamond M. C., Veltman W. A. Effects of differential environments on plasticity of dendrites of cortical pyramidal neurons in adult rats. Exp Neurol. 1978 Dec;62(3):658–677. doi: 10.1016/0014-4886(78)90276-5. [DOI] [PubMed] [Google Scholar]
- VANDERLOOS H. FINE STRUCTURE OF SYNAPSES IN THE CEREBRAL CORTEX. Z Zellforsch Mikrosk Anat. 1963 Sep 18;60:815–825. [PubMed] [Google Scholar]
- Van Harreveld A., Fifkova E. Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp Neurol. 1975 Dec;49(3):736–749. doi: 10.1016/0014-4886(75)90055-2. [DOI] [PubMed] [Google Scholar]
- Walters B. B., Matus A. I. Tubulin in postynaptic junctional lattice. Nature. 1975 Oct 9;257(5526):496–498. doi: 10.1038/257496a0. [DOI] [PubMed] [Google Scholar]
- Wasterlain C. G., Farber D. B. A lasting change in protein phosphorylation associated with septal kindling. Brain Res. 1982 Sep 9;247(1):191–194. doi: 10.1016/0006-8993(82)91050-2. [DOI] [PubMed] [Google Scholar]
- Wasterlain C. G., Farber D. B. Kindling alters the calcium/calmodulin-dependent phosphorylation of synaptic plasma membrane proteins in rat hippocampus. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1253–1257. doi: 10.1073/pnas.81.4.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wesa J. M., Chang F. L., Greenough W. T., West R. W. Synaptic contact curvature: effects of differential rearing on rat occipital cortex. Brain Res. 1982 Jun;256(2):253–257. doi: 10.1016/0165-3806(82)90049-9. [DOI] [PubMed] [Google Scholar]
- West R. W., Greenough W. T. Effect of environmental complexity on cortical synapses of rats: preliminary results. Behav Biol. 1972 Apr;7(2):279–284. doi: 10.1016/s0091-6773(72)80207-4. [DOI] [PubMed] [Google Scholar]
- Wong D. T., Horng J. S. Na+-independent binding of GABA to the triton X-100 treated synaptic membranes from cerebellum of rat brain. Life Sci. 1977 Feb 1;20(3):445–451. doi: 10.1016/0024-3205(77)90386-1. [DOI] [PubMed] [Google Scholar]
- Wood J. G., Wallace R. W., Whitaker J. N., Cheung W. Y. Immunocytochemical localization of calmodulin and a heat-labile calmodulin-binding protein (CaM-BP80) in basal ganglia of mouse brain. J Cell Biol. 1980 Jan;84(1):66–76. doi: 10.1083/jcb.84.1.66. [DOI] [PMC free article] [PubMed] [Google Scholar]