{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,17]],"date-time":"2026-10-17T13:53:49Z","timestamp":1792245229142,"version":"4.4.0"},"reference-count":57,"publisher":"American Association for the Advancement of Science (AAAS)","issue":"5155","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Science"],"published-print":{"date-parts":[[1994,4]]},"abstract":"<jats:p>\n            Several types of calcium channels found in the central nervous system are possible participants in triggering neurotransmitter release. Synaptic transmission between hippocampal CA3 and CA1 neurons was mediated by N-type calcium channels, together with calcium channels whose pharmacology differs from that of L- and P-type channels but resembles that of the Q-type channel encoded by the \u03b1\n            <jats:sub>1A<\/jats:sub>\n            subunit gene. Blockade of either population of channels strongly increased enhancement of synaptic transmission with repetitive stimuli. Even after complete blockade of N-type channels, transmission was strongly modulated by stimulation of neurotransmitter receptors or protein kinase C. These findings suggest a role for \u03b1\n            <jats:sub>1A<\/jats:sub>\n            subunits in synaptic transmission and support the idea that neurotransmitter release may depend on multiple types of calcium channels under physiological conditions.\n          <\/jats:p>","DOI":"10.1126\/science.7832825","type":"journal-article","created":{"date-parts":[[2006,10,6]],"date-time":"2006-10-06T00:01:25Z","timestamp":1160092885000},"page":"107-111","source":"Crossref","is-referenced-by-count":827,"title":["Roles of N-Type and Q-Type Ca\n            <sup>2+<\/sup>\n            Channels in Supporting Hippocampal Synaptic Transmission"],"prefix":"10.1126","volume":"264","author":[{"given":"David B.","family":"Wheeler","sequence":"first","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrew","family":"Randall","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Richard W.","family":"Tsien","sequence":"additional","affiliation":[{"name":"Department of Molecular and Cellular Physiology, Beckman Center for Molecular and Genetic Medicine, Stanford University School of Medicine, Stanford, CA 94305, USA."}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"221","reference":[{"key":"e_1_2_1_1_1","first-page":"381","year":"1984","unstructured":"Alger, B. E., Brain Slice Methods: 381 (1984).","journal-title":"Brain Slice Methods"},{"key":"e_1_2_1_2_1","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/0165-0173(91)90010-6","volume":"16","year":"1991","unstructured":"Anwyl, R., Brain Research Reviews 16: 265 (1991).","journal-title":"Brain Research Reviews"},{"key":"e_1_2_1_3_1","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1146\/annurev.ne.10.030187.003221","volume":"10","year":"1987","unstructured":"AUGUSTINE, G.J., CALCIUM ACTION IN SYNAPTIC TRANSMITTER RELEASE, ANNUAL REVIEW OF NEUROSCIENCE 10: 633 (1987).","journal-title":"ANNUAL REVIEW OF NEUROSCIENCE"},{"key":"e_1_2_1_4_1","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1146\/annurev.ph.51.030189.002055","volume":"51","year":"1989","unstructured":"BEAN, B.P., CLASSES OF CALCIUM CHANNELS IN VERTEBRATE CELLS, ANNUAL REVIEW OF PHYSIOLOGY 51: 367 (1989).","journal-title":"ANNUAL REVIEW OF PHYSIOLOGY"},{"key":"e_1_2_1_5_1","doi-asserted-by":"publisher","DOI":"10.1038\/346724a0"},{"key":"e_1_2_1_6_1","doi-asserted-by":"publisher","DOI":"10.1113\/jphysiol.1986.sp016193"},{"key":"e_1_2_1_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/361031a0"},{"key":"e_1_2_1_8_1","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1113\/jphysiol.1980.sp013133","volume":"299","year":"1980","unstructured":"Creager, R., Journal of Physiology 299: 409 (1980).","journal-title":"Journal of Physiology"},{"key":"e_1_2_1_9_1","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/0304-3940(85)90130-2","volume":"56","year":"1985","unstructured":"DEISZ, R.A., GAMMA-AMINOBUTYRIC ACID-INDUCED DEPRESSION OF CALCIUM CURRENTS OF CHICK SENSORY NEURONS, NEUROSCIENCE LETTERS 56: 205 (1985).","journal-title":"NEUROSCIENCE LETTERS"},{"key":"e_1_2_1_10_1","doi-asserted-by":"crossref","first-page":"218","DOI":"10.1016\/0006-8993(81)90697-1","volume":"207","year":"1981","unstructured":"DINGLEDINE, R, CALCIUM DEPENDENCE OF SYNAPTIC TRANSMISSION IN THE HIPPOCAMPAL SLICE, BRAIN RESEARCH 207: 218 (1981).","journal-title":"BRAIN RESEARCH"},{"key":"e_1_2_1_11_1","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1113\/jphysiol.1967.sp008367","volume":"193","year":"1967","unstructured":"DODGE, F. A., JOURNAL OF PHYSIOLOGY-LONDON 193: 419 (1967).","journal-title":"JOURNAL OF PHYSIOLOGY-LONDON"},{"key":"e_1_2_1_12_1","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/0014-2999(89)90318-X","volume":"174","year":"1989","unstructured":"DUTAR, P, OMEGA-CONOTOXIN GVIA BLOCKS SYNAPTIC TRANSMISSION IN THE CA1 FIELD OF THE HIPPOCAMPUS, EUROPEAN JOURNAL OF PHARMACOLOGY 174: 261 (1989).","journal-title":"EUROPEAN JOURNAL OF PHARMACOLOGY"},{"key":"e_1_2_1_13_1","doi-asserted-by":"crossref","first-page":"455","DOI":"10.1038\/363455a0","volume":"363","year":"1993","unstructured":"ELLINOR, P.T., FUNCTIONAL EXPRESSION OF A RAPIDLY INACTIVATING NEURONAL CALCIUM-CHANNEL, NATURE 363: 455 (1993).","journal-title":"NATURE"},{"key":"e_1_2_1_14_1","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/0304-3940(87)90419-8","volume":"76","year":"1987","unstructured":"GAHWILER, B.H., MUSCARINE AFFECTS CALCIUM-CURRENTS IN RAT HIPPOCAMPAL PYRAMIDAL CELLS-INVITRO, NEUROSCIENCE LETTERS 76: 301 (1987).","journal-title":"NEUROSCIENCE LETTERS"},{"key":"e_1_2_1_15_1","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1113\/jphysiol.1989.sp017592","volume":"411","year":"1989","unstructured":"GROSS, R. A., JOURNAL OF PHYSIOLOGY-LONDON 411: 585 (1989).","journal-title":"JOURNAL OF PHYSIOLOGY-LONDON"},{"key":"e_1_2_1_16_1","doi-asserted-by":"crossref","first-page":"1733","DOI":"10.1111\/j.1476-5381.1991.tb09855.x","volume":"103","year":"1991","unstructured":"HORNE, A.L., THE EFFECT OF OMEGA-CONOTOXIN GVIA ON SYNAPTIC TRANSMISSION WITHIN THE NUCLEUS-ACCUMBENS AND HIPPOCAMPUS OF THE RAT INVITRO, BRITISH JOURNAL OF PHARMACOLOGY 103: 1733 (1991).","journal-title":"BRITISH JOURNAL OF PHARMACOLOGY"},{"key":"e_1_2_1_17_1","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1016\/0304-3940(88)90253-4","volume":"91","year":"1988","unstructured":"KAMIYA, H, SYNTHETIC OMEGA-CONOTOXIN BLOCKS SYNAPTIC TRANSMISSION IN THE HIPPOCAMPUS INVITRO, NEUROSCIENCE LETTERS 91: 84 (1988).","journal-title":"NEUROSCIENCE LETTERS"},{"key":"e_1_2_1_18_1","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1016\/0168-0102(87)90014-9","volume":"4","year":"1987","unstructured":"KASAI, H, NEUROSCI RES 4: 228 (1987).","journal-title":"NEUROSCI RES"},{"key":"e_1_2_1_19_1","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1016\/0896-6273(89)90187-6","volume":"2","year":"1989","unstructured":"LEMOS, J.R., 2 TYPES OF CALCIUM CHANNELS COEXIST IN PEPTIDE-RELEASING VERTEBRATE NERVE-TERMINALS, NEURON 2: 1419 (1989).","journal-title":"NEURON"},{"key":"e_1_2_1_20_1","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/0896-6273(90)90200-Y","volume":"4","year":"1990","unstructured":"LESTER, RAJ, QUISQUALATE RECEPTOR-MEDIATED DEPRESSION OF CALCIUM CURRENTS IN HIPPOCAMPAL-NEURONS, NEURON 4: 741 (1990).","journal-title":"NEURON"},{"key":"e_1_2_1_21_1","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/0166-2236(92)90053-B","volume":"15","year":"1992","unstructured":"LLINAS, R, DISTRIBUTION AND FUNCTIONAL-SIGNIFICANCE OF THE P-TYPE, VOLTAGE-DEPENDENT CA2+ CHANNELS IN THE MAMMALIAN CENTRAL-NERVOUS-SYSTEM, TRENDS IN NEUROSCIENCES 15: 351 (1992).","journal-title":"TRENDS IN NEUROSCIENCES"},{"key":"e_1_2_1_22_1","doi-asserted-by":"publisher","DOI":"10.1038\/321175a0"},{"key":"e_1_2_1_23_1","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1038\/346177a0","volume":"346","year":"1990","unstructured":"MALINOW, R, PRESYNAPTIC ENHANCEMENT SHOWN BY WHOLE-CELL RECORDINGS OF LONG-TERM POTENTIATION IN HIPPOCAMPAL SLICES, NATURE 346: 177 (1990).","journal-title":"NATURE"},{"key":"e_1_2_1_24_1","doi-asserted-by":"crossref","first-page":"1451","DOI":"10.1152\/jn.1993.70.4.1451","volume":"70","year":"1993","unstructured":"MANABE, T, MODULATION OF SYNAPTIC TRANSMISSION AND LONG-TERM POTENTIATION - EFFECTS ON PAIRED-PULSE FACILITATION AND EPSC VARIANCE IN THE CA1 REGION OF THE HIPPOCAMPUS, JOURNAL OF NEUROPHYSIOLOGY 70: 1451 (1993).","journal-title":"JOURNAL OF NEUROPHYSIOLOGY"},{"key":"e_1_2_1_25_1","first-page":"4327","volume":"84","year":"1987","unstructured":"MCCLESKEY, E.W., OMEGA-CONOTOXIN - DIRECT AND PERSISTENT BLOCKADE OF SPECIFIC TYPES OF CALCIUM CHANNELS IN NEURONS BUT NOT MUSCLE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 84: 4327 (1987).","journal-title":"PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"},{"key":"e_1_2_1_26_1","first-page":"673P","article-title":"Calcium channel activator properties in a novel non-dihydropyridine-FPL 64176","volume":"98","year":"1989","unstructured":"McKechnie, K., Calcium channel activator properties in a novel non-dihydropyridine-FPL 64176, British Journal of Pharmacology 98 1: 673P (1989).","journal-title":"British Journal of Pharmacology"},{"key":"e_1_2_1_27_1","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1016\/0960-9822(93)90364-T","volume":"3","year":"1993","unstructured":"MILLER, R.J., A TALE OF 2 TOXINS, CURRENT BIOLOGY 3: 481 (1993).","journal-title":"CURRENT BIOLOGY"},{"key":"e_1_2_1_28_1","first-page":"97","year":"1990","unstructured":"Miller, R. J., Intracellular Calcium Regulation: 97 (1990).","journal-title":"Intracellular Calcium Regulation"},{"key":"e_1_2_1_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/0896-6273(92)90223-Z"},{"key":"e_1_2_1_30_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/0896-6273(93)90236-K","volume":"10","year":"1993","unstructured":"MINTZ, I.M., NEURON 10: 1 (1993).","journal-title":"NEURON"},{"key":"e_1_2_1_31_1","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.1016\/0028-3908(93)90010-Z","volume":"32","year":"1993","unstructured":"MINTZ, I.M., BLOCK OF CALCIUM CHANNELS IN RAT NEURONS BY SYNTHETIC OMEGA-AGA-IVA, NEUROPHARMACOLOGY 32: 1161 (1993).","journal-title":"NEUROPHARMACOLOGY"},{"key":"e_1_2_1_32_1","doi-asserted-by":"crossref","first-page":"398","DOI":"10.1038\/350398a0","volume":"350","year":"1991","unstructured":"MORI, Y, PRIMARY STRUCTURE AND FUNCTIONAL EXPRESSION FROM COMPLEMENTARY-DNA OF A BRAIN CALCIUM-CHANNEL, NATURE 350: 398 (1991).","journal-title":"NATURE"},{"key":"e_1_2_1_33_1","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/0006-8993(88)91124-9","volume":"447","year":"1988","unstructured":"MULKEEN, D, THE EFFECTS OF EXTERNAL CALCIUM ON LONG-TERM POTENTIATION IN THE RAT HIPPOCAMPAL SLICE, BRAIN RESEARCH 447: 234 (1988).","journal-title":"BRAIN RESEARCH"},{"key":"e_1_2_1_34_1","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/0006-8993(89)91631-4","volume":"479","year":"1989","unstructured":"MULLER, D, EVIDENCE THAT CHANGES IN PRESYNAPTIC CALCIUM CURRENTS ARE NOT RESPONSIBLE FOR LONG-TERM POTENTIATION IN HIPPOCAMPUS, BRAIN RESEARCH 479: 290 (1989).","journal-title":"BRAIN RESEARCH"},{"key":"e_1_2_1_35_1","doi-asserted-by":"crossref","first-page":"7","DOI":"10.1016\/0014-5793(92)81038-N","volume":"308","year":"1992","unstructured":"NIIDOME, T, MOLECULAR-CLONING AND CHARACTERIZATION OF A NOVEL CALCIUM-CHANNEL FROM RABBIT BRAIN, FEBS LETTERS 308: 7 (1992).","journal-title":"FEBS LETTERS"},{"key":"e_1_2_1_36_1","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1113\/jphysiol.1993.sp019900","volume":"471","year":"1993","unstructured":"PARFITT, K. D., JOURNAL OF PHYSIOLOGY-LONDON 471: 245 (1993).","journal-title":"JOURNAL OF PHYSIOLOGY-LONDON"},{"key":"e_1_2_1_37_1","first-page":"44","volume":"8","year":"1993","unstructured":"RANDALL, A.D., FUNCT NEUROL S 8: 44 (1993).","journal-title":"FUNCT NEUROL S"},{"key":"e_1_2_1_38_1","first-page":"1478","volume":"19","year":"1993","unstructured":"RANDALL, A.D., SOC NEUR ABSTR 19: 1478 (1993).","journal-title":"SOC NEUR ABSTR"},{"key":"e_1_2_1_39_1","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1016\/0896-6273(91)90362-4","volume":"6","year":"1991","unstructured":"REGAN, L.J., CA2+ CHANNELS IN RAT CENTRAL AND PERIPHERAL NEURONS - HIGH-THRESHOLD CURRENT RESISTANT TO DIHYDROPYRIDINE BLOCKERS AND OMEGA-CONOTOXIN, NEURON 6: 269 (1991).","journal-title":"NEURON"},{"key":"e_1_2_1_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/0896-6273(93)90185-T"},{"key":"e_1_2_1_41_1","doi-asserted-by":"crossref","first-page":"1139","DOI":"10.1016\/0896-6273(92)90134-Y","volume":"8","year":"1992","unstructured":"SCHOLZ, K.P., INHIBITION OF QUANTAL TRANSMITTER RELEASE IN THE ABSENCE OF CALCIUM INFLUX BY A G-PROTEIN LINKED ADENOSINE RECEPTOR AT HIPPOCAMPAL SYNAPSES, NEURON 8: 1139 (1992).","journal-title":"NEURON"},{"key":"e_1_2_1_42_1","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1016\/0959-4388(92)90111-W","volume":"2","year":"1992","unstructured":"SNUTCH, T.P., CURR OPIN NEUROBIOL 2: 247 (1992).","journal-title":"CURR OPIN NEUROBIOL"},{"key":"e_1_2_1_43_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.8388125"},{"key":"e_1_2_1_44_1","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/361165a0","volume":"361","year":"1993","unstructured":"SWARTZ, K.J., PROTEIN-KINASE-C MODULATES GLUTAMATE RECEPTOR INHIBITION OF CA2+ CHANNELS AND SYNAPTIC TRANSMISSION, NATURE 361: 165 (1993).","journal-title":"NATURE"},{"key":"e_1_2_1_45_1","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1016\/0896-6273(93)90186-U","volume":"11","year":"1993","unstructured":"SWARTZ, K.J., MODULATION OF CA2+ CHANNELS BY PROTEIN-KINASE-C IN RAT CENTRAL AND PERIPHERAL NEURONS - DISRUPTION OF G-PROTEIN-MEDIATED INHIBITION, NEURON 11: 305 (1993).","journal-title":"NEURON"},{"key":"e_1_2_1_46_1","first-page":"1478","volume":"19","year":"1993","unstructured":"SWARTZ, K.J., SOC NEUR ABSTR 19: 1478 (1993).","journal-title":"SOC NEUR ABSTR"},{"key":"e_1_2_1_47_1","doi-asserted-by":"publisher","DOI":"10.1038\/366156a0"},{"key":"e_1_2_1_48_1","doi-asserted-by":"publisher","DOI":"10.1016\/0166-2236(88)90194-4"},{"key":"e_1_2_1_49_1","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/0165-6147(91)90595-J","volume":"12","year":"1991","unstructured":"TSIEN, R.W., MOLECULAR DIVERSITY OF VOLTAGE-DEPENDENT CA2+ CHANNELS, TRENDS IN PHARMACOLOGICAL SCIENCES 12: 349 (1991).","journal-title":"TRENDS IN PHARMACOLOGICAL SCIENCES"},{"key":"e_1_2_1_50_1","first-page":"9518","volume":"90","year":"1993","unstructured":"TURNER, T.J., MULTIPLE CA2+ CHANNEL TYPES COEXIST TO REGULATE SYNAPTOSOMAL NEUROTRANSMITTER RELEASE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 90: 9518 (1993).","journal-title":"PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA"},{"key":"e_1_2_1_51_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1357749"},{"key":"e_1_2_1_52_1","unstructured":"WHEELER D.B. unpublished data."},{"key":"e_1_2_1_53_1","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1523\/JNEUROSCI.14-02-00645.1994","volume":"14","year":"1994","unstructured":"WU, L.G., PRESYNAPTIC CALCIUM IS INCREASED DURING NORMAL SYNAPTIC TRANSMISSION AND PAIRED-PULSE FACILITATION, BUT NOT IN LONG-TERM POTENTIATION IN AREA CA1 OF HIPPOCAMPUS, JOURNAL OF NEUROSCIENCE 14: 645 (1994).","journal-title":"JOURNAL OF NEUROSCIENCE"},{"key":"e_1_2_1_54_1","first-page":"1518","volume":"19","year":"1993","unstructured":"WU, L.G., SOC NEUR ABSTR 19: 1518 (1993).","journal-title":"SOC NEUR ABSTR"},{"key":"e_1_2_1_55_1","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/0896-6273(93)90305-B","volume":"10","year":"1993","unstructured":"YANG, J, ENHANCEMENT OF N-TYPE AND L-TYPE CALCIUM-CHANNEL CURRENTS BY PROTEIN-KINASE-C IN FROG SYMPATHETIC NEURONS, NEURON 10: 127 (1993).","journal-title":"NEURON"},{"key":"e_1_2_1_56_1","doi-asserted-by":"crossref","first-page":"1075","DOI":"10.1016\/0028-3908(93)90003-L","volume":"32","year":"1993","unstructured":"ZHANG, J.F., DISTINCTIVE PHARMACOLOGY AND KINETICS OF CLONED NEURONAL CA2+ CHANNELS AND THEIR POSSIBLE COUNTERPARTS IN MAMMALIAN CNS NEURONS, NEUROPHARMACOLOGY 32: 1075 (1993).","journal-title":"NEUROPHARMACOLOGY"},{"key":"e_1_2_1_57_1","unstructured":"ZHANG J.F. unpublished data."}],"container-title":["Science"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.science.org\/doi\/pdf\/10.1126\/science.7832825","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,1,15]],"date-time":"2024-01-15T05:25:38Z","timestamp":1705296338000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.science.org\/doi\/10.1126\/science.7832825"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1994,4]]},"references-count":57,"journal-issue":{"issue":"5155","published-print":{"date-parts":[[1994,4]]}},"alternative-id":["10.1126\/science.7832825"],"URL":"https:\/\/doi.org\/10.1126\/science.7832825","relation":{},"ISSN":["0036-8075","1095-9203"],"issn-type":[{"value":"0036-8075","type":"print"},{"value":"1095-9203","type":"electronic"}],"subject":[],"published":{"date-parts":[[1994,4]]}}}