Abstract
Postsynaptic density (PSD) fractions were isolated from the cerebral cortices of control and kindled rats and assayed for glutamate and gamma-aminobutyric acid-binding capacities and for the Ca2+/calmodulin-dependent protein kinase. Glutamate binding was found to be increased by approximately 50% in the PSDs isolated from kindled rats as compared to controls; this increase was almost completely from an increase in Bmax; Kd decreased only slightly. Studies with inhibitors indicate that the receptors involved were of the N-methyl-D-aspartate and quisqualate types. PSDs isolated from control and kindled rats did not differ in gamma-aminobutyric acid or flunitrazepam binding. The in vitro autophosphorylation of the Ca2+/calmodulin-dependent protein kinase was depressed by 45-76% in PSDs isolated from kindled rats as compared to controls, with little change in amount of the kinase. Therefore, we infer that (i) the kindled state is associated with an increase in glutamate activation of postsynaptic sites, allowing Ca2+ to enter dendritic spines, (ii) a change has occurred in activity of the protein kinase, which is the major cerebral cortex PSD protein, and (iii) perhaps major alterations in the PSD are a concomitant to the long-lasting nature of the kindled state.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bank B., Gurd J. W., Chute D. L. Decreased phosphorylation of synaptic glycoproteins following hippocampal kindling. Brain Res. 1986 Dec 10;399(2):390–394. doi: 10.1016/0006-8993(86)91534-9. [DOI] [PubMed] [Google Scholar]
- Baudry M., Oliver M., Creager R., Wieraszko A., Lynch G. Increase in glutamate receptors following repetitive electrical stimulation in hippocampal slices. Life Sci. 1980 Jul 28;27(4):325–330. doi: 10.1016/0024-3205(80)90200-3. [DOI] [PubMed] [Google Scholar]
- Brown T. H., Chapman P. F., Kairiss E. W., Keenan C. L. Long-term synaptic potentiation. Science. 1988 Nov 4;242(4879):724–728. doi: 10.1126/science.2903551. [DOI] [PubMed] [Google Scholar]
- Burnham W. M. Primary and "transfer" seizure development in the kindled rat. Can J Neurol Sci. 1975 Nov;2(4):417–428. doi: 10.1017/s0317167100020564. [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]
- Bär P. R., Tielen A. M., Lopes Da Silva F. H., Zwiers H., Gispen W. H. Membrane phosphoproteins of rat hippocampus: sensitivity to tetanic stimulation and enkephalin. Brain Res. 1982 Aug 5;245(1):69–79. doi: 10.1016/0006-8993(82)90340-7. [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., 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]
- Cavalheiro E. A., Turski L. Intrastriatal N-methyl-D-aspartate prevents amygdala kindled seizures in rats. Brain Res. 1986 Jul 2;377(1):173–176. doi: 10.1016/0006-8993(86)91204-7. [DOI] [PubMed] [Google Scholar]
- Chang F. L., Greenough W. T. Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res. 1984 Aug 20;309(1):35–46. doi: 10.1016/0006-8993(84)91008-4. [DOI] [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]
- Colbran R. J., Fong Y. L., Schworer C. M., Soderling T. R. Regulatory interactions of the calmodulin-binding, inhibitory, and autophosphorylation domains of Ca2+/calmodulin-dependent protein kinase II. J Biol Chem. 1988 Dec 5;263(34):18145–18151. [PubMed] [Google Scholar]
- Crunelli V., Forda S., Kelly J. S. Blockade of amino acid-induced depolarizations and inhibition of excitatory post-synaptic potentials in rat dentate gyrus. J Physiol. 1983 Aug;341:627–640. doi: 10.1113/jphysiol.1983.sp014829. [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]
- 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]
- Fanelli R. J., McNamara J. O. Effects of age on kindling and kindled seizure-induced increase of benzodiazepine receptor binding. Brain Res. 1986 Jan 1;362(1):17–22. doi: 10.1016/0006-8993(86)91393-4. [DOI] [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]
- Fujisawa H., Yamauchi T., Nakata H., Okuno S. Role of calmodulin in neurotransmitter synthesis. Fed Proc. 1984 Dec;43(15):3011–3014. [PubMed] [Google Scholar]
- Geinisman Y., Morrell F., deToledo-Morrell L. Increase in the relative proportion of perforated axospinous synapses following hippocampal kindling is specific for the synaptic field of stimulated axons. Brain Res. 1990 Jan 22;507(2):325–331. doi: 10.1016/0006-8993(90)90291-i. [DOI] [PubMed] [Google Scholar]
- Geinisman Y., Morrell F., deToledo-Morrell L. Remodeling of synaptic architecture during hippocampal "kindling". Proc Natl Acad Sci U S A. 1988 May;85(9):3260–3264. doi: 10.1073/pnas.85.9.3260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geinisman Y., de Toledo-Morrell L., Morrell F. Loss of perforated synapses in the dentate gyrus: morphological substrate of memory deficit in aged rats. Proc Natl Acad Sci U S A. 1986 May;83(9):3027–3031. doi: 10.1073/pnas.83.9.3027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gilbert M. E. The NMDA-receptor antagonist, MK-801, suppresses limbic kindling and kindled seizures. Brain Res. 1988 Oct 25;463(1):90–99. doi: 10.1016/0006-8993(88)90530-6. [DOI] [PubMed] [Google Scholar]
- Goddard G. V. Analysis of avoidance conditioning following cholinergic stimulation of amygdala in rats. J Comp Physiol Psychol. 1969 Jun;68(2):1–18. doi: 10.1037/h0027504. [DOI] [PubMed] [Google Scholar]
- Goddard G. V., Douglas R. M. Does the engram of kindling model the engram of normal long term memory? Can J Neurol Sci. 1975 Nov;2(4):385–394. doi: 10.1017/s0317167100020539. [DOI] [PubMed] [Google Scholar]
- Goddard G. V., McIntyre D. C., Leech C. K. A permanent change in brain function resulting from daily electrical stimulation. Exp Neurol. 1969 Nov;25(3):295–330. doi: 10.1016/0014-4886(69)90128-9. [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]
- Goldenring J. R., Wasterlain C. G., Oestreicher A. B., de Graan P. N., Farber D. B., Glaser G., DeLorenzo R. J. Kindling induces a long-lasting change in the activity of a hippocampal membrane calmodulin-dependent protein kinase system. Brain Res. 1986 Jul 2;377(1):47–53. doi: 10.1016/0006-8993(86)91189-3. [DOI] [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]
- 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., McGuinness T. L., Greengard P. Evidence that the major postsynaptic density protein is a component of a Ca2+/calmodulin-dependent protein kinase. Proc Natl Acad Sci U S A. 1984 Feb;81(3):945–949. doi: 10.1073/pnas.81.3.945. [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]
- Kwiatkowski A. P., Shell D. J., King M. M. The role of autophosphorylation in activation of the type II calmodulin-dependent protein kinase. J Biol Chem. 1988 May 15;263(14):6484–6486. [PubMed] [Google Scholar]
- LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
- Le Vine H., 3rd, Sahyoun N. E., Cuatrecasas P. Binding of calmodulin to the neuronal cytoskeletal protein kinase type II cooperatively stimulates autophosphorylation. Proc Natl Acad Sci U S A. 1986 Apr;83(7):2253–2257. doi: 10.1073/pnas.83.7.2253. [DOI] [PMC free article] [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]
- Lickteig R., Shenolikar S., Denner L., Kelly P. T. Regulation of Ca2+/calmodulin-dependent protein kinase II by Ca2+/calmodulin-independent autophosphorylation. J Biol Chem. 1988 Dec 15;263(35):19232–19239. [PubMed] [Google Scholar]
- Lisman J. E., Goldring M. A. Feasibility of long-term storage of graded information by the Ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density. Proc Natl Acad Sci U S A. 1988 Jul;85(14):5320–5324. doi: 10.1073/pnas.85.14.5320. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Llinás R., McGuinness T. L., Leonard C. S., Sugimori M., Greengard P. Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. Proc Natl Acad Sci U S A. 1985 May;82(9):3035–3039. doi: 10.1073/pnas.82.9.3035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lynch G., Halpain S., Baudry M. Effects of high-frequency synaptic stimulation on glumate receptor binding studied with a modified in vitro hippocampal slice preparation. Brain Res. 1982 Jul 22;244(1):101–111. doi: 10.1016/0006-8993(82)90908-8. [DOI] [PubMed] [Google Scholar]
- McIntyre D. C., Racine R. J. Kindling mechanisms: current progress on an experimental epilepsy model. Prog Neurobiol. 1986;27(1):1–12. doi: 10.1016/0301-0082(86)90010-9. [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., Peper A. M., Patrone V. Repeated seizures induce long-term increase in hippocampal benzodiazepine receptors. Proc Natl Acad Sci U S A. 1980 May;77(5):3029–3032. doi: 10.1073/pnas.77.5.3029. [DOI] [PMC free article] [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]
- Miller S. G., Kennedy M. B. Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch. Cell. 1986 Mar 28;44(6):861–870. doi: 10.1016/0092-8674(86)90008-5. [DOI] [PubMed] [Google Scholar]
- Mody I., Heinemann U. NMDA receptors of dentate gyrus granule cells participate in synaptic transmission following kindling. Nature. 1987 Apr 16;326(6114):701–704. doi: 10.1038/326701a0. [DOI] [PubMed] [Google Scholar]
- Monaghan D. T., Cotman C. W. Identification and properties of N-methyl-D-aspartate receptors in rat brain synaptic plasma membranes. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7532–7536. doi: 10.1073/pnas.83.19.7532. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Monaghan D. T., Holets V. R., Toy D. W., Cotman C. W. Anatomical distributions of four pharmacologically distinct 3H-L-glutamate binding sites. Nature. 1983 Nov 10;306(5939):176–179. doi: 10.1038/306176a0. [DOI] [PubMed] [Google Scholar]
- Morrell F., Tsuru N. Kindling in the frog: development of spontaneous epileptiform activity. Electroencephalogr Clin Neurophysiol. 1976 Jan;40(1):1–11. doi: 10.1016/0013-4694(76)90174-7. [DOI] [PubMed] [Google Scholar]
- Moshkov D. A., Petrovskaia L. L., Bragin A. G. Posttetanicheskie izmeneniia v ul'trastrukture gigantskikh shipikovskikh sinapsov polia CA3 gippokampa. Dokl Akad Nauk SSSR. 1977;237(6):1525–1528. [PubMed] [Google Scholar]
- Murphy S. N., Miller R. J. A glutamate receptor regulates Ca2+ mobilization in hippocampal neurons. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8737–8741. doi: 10.1073/pnas.85.22.8737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Niznik H. B., Burnham W. M., Kish S. J. Benzodiazepine receptor binding following amygdala-kindled convulsions: differing results in washed and unwashed brain membranes. J Neurochem. 1984 Dec;43(6):1732–1736. doi: 10.1111/j.1471-4159.1984.tb06101.x. [DOI] [PubMed] [Google Scholar]
- Olverman H. J., Jones A. W., Watkins J. C. L-glutamate has higher affinity than other amino acids for [3H]-D-AP5 binding sites in rat brain membranes. Nature. 1984 Feb 2;307(5950):460–462. doi: 10.1038/307460a0. [DOI] [PubMed] [Google Scholar]
- Ouimet C. C., McGuinness T. L., Greengard P. Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5604–5608. doi: 10.1073/pnas.81.17.5604. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Patel J., Marangos P. J., Contel N., Gardner G., Post R. M. Increased phosphorylation of a membrane protein consequent to amygdaloid kindling. J Neurochem. 1984 Jul;43(1):169–173. doi: 10.1111/j.1471-4159.1984.tb06693.x. [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]
- Pinel J. P., Rovner L. I. Electrode placement and kindling-induced experimental epilepsy. Exp Neurol. 1978 Jan 15;58(2):335–346. doi: 10.1016/0014-4886(78)90145-0. [DOI] [PubMed] [Google Scholar]
- Racine R. J. Modification of seizure activity by electrical stimulation. I. After-discharge threshold. Electroencephalogr Clin Neurophysiol. 1972 Mar;32(3):269–279. doi: 10.1016/0013-4694(72)90176-9. [DOI] [PubMed] [Google Scholar]
- Racine R. J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972 Mar;32(3):281–294. doi: 10.1016/0013-4694(72)90177-0. [DOI] [PubMed] [Google Scholar]
- Racine R. J. Modification of seizure activity by electrical stimulation: cortical areas. Electroencephalogr Clin Neurophysiol. 1975 Jan;38(1):1–12. doi: 10.1016/0013-4694(75)90204-7. [DOI] [PubMed] [Google Scholar]
- Racine R., Tuff L., Zaide J. Kindling, unit discharge patterns and neural plasticity. Can J Neurol Sci. 1975 Nov;2(4):395–405. doi: 10.1017/s0317167100020540. [DOI] [PubMed] [Google Scholar]
- Rosenthal H. E. A graphic method for the determination and presentation of binding parameters in a complex system. Anal Biochem. 1967 Sep;20(3):525–532. doi: 10.1016/0003-2697(67)90297-7. [DOI] [PubMed] [Google Scholar]
- Saitoh T., Schwartz J. H. Phosphorylation-dependent subcellular translocation of a Ca2+/calmodulin-dependent protein kinase produces an autonomous enzyme in Aplysia neurons. J Cell Biol. 1985 Mar;100(3):835–842. doi: 10.1083/jcb.100.3.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schrama L. H., de Graan P. N., Zwiers H., Gispen W. H. Comparison of a 52-kDa phosphoprotein from synaptic plasma membranes related to long-term potentiation and the major coated vesicle phosphoprotein. J Neurochem. 1986 Dec;47(6):1843–1848. doi: 10.1111/j.1471-4159.1986.tb13097.x. [DOI] [PubMed] [Google Scholar]
- Shields S. M., Vernon P. J., Kelly P. T. Autophosphorylation of calmodulin-kinase II in synaptic junctions modulates endogenous kinase activity. J Neurochem. 1984 Dec;43(6):1599–1609. doi: 10.1111/j.1471-4159.1984.tb06084.x. [DOI] [PubMed] [Google Scholar]
- Shin C., Pedersen H. B., McNamara J. O. gamma-Aminobutyric acid and benzodiazepine receptors in the kindling model of epilepsy: a quantitative radiohistochemical study. J Neurosci. 1985 Oct;5(10):2696–2701. doi: 10.1523/JNEUROSCI.05-10-02696.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siekevitz P. The postsynaptic density: a possible role in long-lasting effects in the central nervous system. Proc Natl Acad Sci U S A. 1985 May;82(10):3494–3498. doi: 10.1073/pnas.82.10.3494. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sloviter R. S., Dempster D. W. "Epileptic" brain damage is replicated qualitatively in the rat hippocampus by central injection of glutamate or aspartate but not by GABA or acetylcholine. Brain Res Bull. 1985 Jul;15(1):39–60. doi: 10.1016/0361-9230(85)90059-0. [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]
- 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]
- Wada J. A., Osawa T., Mizoguchi T. Recurrent spontaneous seizure state induced by prefrontal kindling in senegalese baboons, Papio papio. Can J Neurol Sci. 1975 Nov;2(4):477–492. doi: 10.1017/s031716710002062x. [DOI] [PubMed] [Google Scholar]
- Wake A., Wada J. A. Transfer and interference in amygdaloid kindling in cats. Can J Neurol Sci. 1977 Feb;4(1):5–11. [PubMed] [Google Scholar]
- Walaas S. I., Gorelick F. S., Greengard P. Presence of calcium/calmodulin-dependent protein kinase II in nerve terminals of rat brain. Synapse. 1989;3(4):356–362. doi: 10.1002/syn.890030409. [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]
- Wasterlain C. G., Jonec V. Chemical kindling by muscarinic amygdaloid stimulation in the rat. Brain Res. 1983 Jul 25;271(2):311–323. doi: 10.1016/0006-8993(83)90293-7. [DOI] [PubMed] [Google Scholar]
- Wu K., Carlin R., Siekevitz P. Binding of L-[3H]glutamate to fresh or frozen synaptic membrane and postsynaptic density fractions isolated from cerebral cortex and cerebellum of fresh or frozen canine brain. J Neurochem. 1986 Mar;46(3):831–841. doi: 10.1111/j.1471-4159.1986.tb13047.x. [DOI] [PubMed] [Google Scholar]
- Wu K., Sachs L., Carlin R. K., Siekevitz P. Characteristics of a Ca2+/calmodulin-dependent binding of the Ca2+ channel antagonist, nitrendipine, to a postsynaptic density fraction isolated from canine cerebral cortex. Brain Res. 1986 Nov;387(2):167–184. doi: 10.1016/0169-328x(86)90008-2. [DOI] [PubMed] [Google Scholar]
- Wu K., Siekevitz P. Neurochemical characteristics of a postsynaptic density fraction isolated from adult canine hippocampus. Brain Res. 1988 Aug 2;457(1):98–112. doi: 10.1016/0006-8993(88)90061-3. [DOI] [PubMed] [Google Scholar]
- Yeh G. C., Bonhaus D. W., Nadler J. V., McNamara J. O. N-methyl-D-aspartate receptor plasticity in kindling: quantitative and qualitative alterations in the N-methyl-D-aspartate receptor-channel complex. Proc Natl Acad Sci U S A. 1989 Oct;86(20):8157–8160. doi: 10.1073/pnas.86.20.8157. [DOI] [PMC free article] [PubMed] [Google Scholar]