DOI: 10.1126/science.3495885. The Dynamics of Free Calcium in Dendritic Spines in Response to Repetitive Synaptic Input

The Dynamics of Free Calcium in Dendritic Spines in Response to Repetitive Synaptic Input

10.1126/science.3495885

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Increased levels of intracellular calcium at either pre- or postsynaptic sites are thought to precede changes in synaptic strength. Thus, to induce long-term potentiation in the hippocampus, periods of intense synaptic stimulation would have to transiently raise the levels of cytosolic calcium at postsynaptic sites—dendritic spines in the majority of cases. Since direct experimental verification of this hypothesis is not possible at present, calcium levels have been studied by numerically solving the appropriate electro-diffusion equations for two different postsynaptic structures. Under the assumption that voltage-dependent calcium channels are present on dendritic spines, free intracellular calcium in spines can reach micromolar levels after as few as seven spikes in 20 milliseconds. Moreover, a short, but high-frequency, burst of presynaptic activity is more effective in raising levels of calcium and especially of the calcium-calmodulin complex than sustained low-frequency activity. This behavior is different from that seen at the soma of a typical vertebrate neuron.

Bibliography

Gamble, E., & Koch, C. (1987). The Dynamics of Free Calcium in Dendritic Spines in Response to Repetitive Synaptic Input. Science, 236(4806), 1311â1315.

Authors 2

Edward Gamble (first)
Christof Koch (additional)

References 47 Referenced 149

10.1126/science.6328653
ADAMS, P.R., ADVANCES IN NEUROLOGY 44: 137 (1986). / ADVANCES IN NEUROLOGY (1986)
ADAMS, P.R., SLOW SYNAPTIC TRANSMISSION IN FROG SYMPATHETIC-GANGLIA, JOURNAL OF EXPERIMENTAL BIOLOGY 124: 259 (1986). (10.1242/jeb.124.1.259) / JOURNAL OF EXPERIMENTAL BIOLOGY (1986)
10.1016/S0006-3495(85)83861-3
10.1126/science.6093258
BAKER, P.F., J PHYSL LONDON 260: 24 (1976). / J PHYSL LONDON (1976)
BARRIONUEVO, G, ASSOCIATIVE LONG-TERM POTENTIATION IN HIPPOCAMPAL SLICES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES 80: 7347 (1983). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA-BIOLOGICAL SCIENCES (1983)
COSS, R.G., THE FUNCTION OF DENDRITIC SPINES - A REVIEW OF THEORETICAL ISSUES, BEHAVIORAL AND NEURAL BIOLOGY 44: 151 (1985). (10.1016/S0163-1047(85)90170-0) / BEHAVIORAL AND NEURAL BIOLOGY (1985)
10.1038/312101a0
CRICK, F, DO DENDRITIC SPINES TWITCH, TRENDS IN NEUROSCIENCES 5: 44 (1982). (10.1016/0166-2236(82)90020-0) / TRENDS IN NEUROSCIENCES (1982)
DINGLEDINE, R, N-METHYL ASPARTATE ACTIVATES VOLTAGE-DEPENDENT CALCIUM CONDUCTANCE IN RAT HIPPOCAMPAL PYRAMIDAL CELLS, JOURNAL OF PHYSIOLOGY-LONDON 343: 385 (1983). (10.1113/jphysiol.1983.sp014899) / JOURNAL OF PHYSIOLOGY-LONDON (1983)
DIPOLO, R, THE CALCIUM-PUMP AND SODIUM-CALCIUM EXCHANGE IN SQUID AXONS, ANNUAL REVIEW OF PHYSIOLOGY 45: 313 (1983). (10.1146/annurev.ph.45.030183.001525) / ANNUAL REVIEW OF PHYSIOLOGY (1983)
ECCLES, J.C., CALCIUM IN LONG-TERM POTENTIATION AS A MODEL FOR MEMORY, NEUROSCIENCE 10: 1071 (1983). (10.1016/0306-4522(83)90100-8) / NEUROSCIENCE (1983)
FIFKOVA, E, CALCIUM IN THE SPINE APPARATUS OF DENDRITIC SPINES IN THE DENTATE MOLECULAR LAYER, BRAIN RESEARCH 266: 163 (1983). (10.1016/0006-8993(83)91322-7) / BRAIN RESEARCH (1983)
HALLIWELL, J.V., J PHYSIOL-LONDON 341: 10 (1983). / J PHYSIOL-LONDON (1983)
HALLIWELL, J.V., VOLTAGE-CLAMP ANALYSIS OF MUSCARINIC EXCITATION IN HIPPOCAMPAL-NEURONS, BRAIN RESEARCH 250: 71 (1982). (10.1016/0006-8993(82)90954-4) / BRAIN RESEARCH (1982)
HARRIS, E.W., LONG-TERM POTENTIATION OF GUINEA-PIG MOSSY FIBER RESPONSES IS NOT BLOCKED BY N-METHYL D-ASPARTATE ANTAGONISTS, NEUROSCIENCE LETTERS 70: 132 (1986). (10.1016/0304-3940(86)90451-9) / NEUROSCIENCE LETTERS (1986)
JACK J.J. ELECTRIC CURRENT FLO (1975).
JACOBSON, S, DIMENSIONS OF DENDRITIC SPINE IN SENSORIMOTOR CORTEX OF RAT CAT SQUIRREL MONKEY AND MAN, JOURNAL OF COMPARATIVE NEUROLOGY 129: 49 (1967). (10.1002/cne.901290104) / JOURNAL OF COMPARATIVE NEUROLOGY (1967)
JAHNSEN, H, IONIC BASIS FOR THE ELECTRORESPONSIVENESS AND OSCILLATORY PROPERTIES OF GUINEA-PIG THALAMIC NEURONS INVITRO, JOURNAL OF PHYSIOLOGY-LONDON 349: 227 (1984). (10.1113/jphysiol.1984.sp015154) / JOURNAL OF PHYSIOLOGY-LONDON (1984)
KANDEL, E.R., CALCIUM AND THE CONTROL OF SYNAPTIC STRENGTH BY LEARNING, NATURE 293: 697 (1981). (10.1038/293697a0) / NATURE (1981)
10.1073/pnas.83.14.5326
KOCH, C, A THEORETICAL-ANALYSIS OF ELECTRICAL-PROPERTIES OF SPINES, PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES 218: 455 (1983). / PROCEEDINGS OF THE ROYAL SOCIETY OF LONDON SERIES B-BIOLOGICAL SCIENCES (1983)
KOCH C unpublished data.
KRNJEVIC, K, CHANGES IN FREE CALCIUM-ION CONCENTRATION RECORDED INSIDE HIPPOCAMPAL PYRAMIDAL CELLS INSITU, BRAIN RESEARCH 374: 1 (1986). (10.1016/0006-8993(86)90388-4) / BRAIN RESEARCH (1986)
LISMAN, J.E., A MECHANISM FOR MEMORY STORAGE INSENSITIVE TO MOLECULAR TURNOVER - A BISTABLE AUTOPHOSPHORYLATING KINASE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 3055 (1985). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1985)
10.1038/305719a0
10.1126/science.6144182
10.1038/321519a0
10.1038/320529a0
MILLER, J.P., SYNAPTIC AMPLIFICATION BY ACTIVE MEMBRANE IN DENDRITIC SPINES, BRAIN RESEARCH 325: 325 (1985). (10.1016/0006-8993(85)90333-6) / BRAIN RESEARCH (1985)
MILLER, S.G., REGULATION OF BRAIN TYPE-II CA-2+ CALMODULIN-DEPENDENT PROTEIN-KINASE BY AUTOPHOSPHORYLATION - A CA-2+-TRIGGERED MOLECULAR SWITCH, CELL 44: 861 (1986). (10.1016/0092-8674(86)90008-5) / CELL (1986)
MONAGHAN, D.T., DISTRIBUTION OF N-METHYL-D-ASPARTATE-SENSITIVE L-[H-3]GLUTAMATE-BINDING SITES IN RAT-BRAIN, JOURNAL OF NEUROSCIENCE 5: 2909 (1985). (10.1523/JNEUROSCI.05-11-02909.1985) / JOURNAL OF NEUROSCIENCE (1985)
PONGRACZ, F, THE FUNCTION OF DENDRITIC SPINES - A THEORETICAL-STUDY, NEUROSCIENCE 15: 933 (1985). (10.1016/0306-4522(85)90244-1) / NEUROSCIENCE (1985)
Qian N. Cellular Mechanisms of Conditioning and Behavioral Plasticity (1988).
RALL, W, STUDIES NEUROPHYSIOL: 203 (1978). / STUDIES NEUROPHYSIOL (1978)
RASMUSSEN, H, CALCIUM MESSENGER SYSTEM - AN INTEGRATED VIEW, PHYSIOLOGICAL REVIEWS 64: 938 (1984). (10.1152/physrev.1984.64.3.938) / PHYSIOLOGICAL REVIEWS (1984)
ROBINSON H MIT779 ART INT LAB M (1984).
10.1016/S0006-3495(86)83465-8
SCHOLEY, J.M., REGULATION OF NON-MUSCLE MYOSIN ASSEMBLY BY CALMODULIN-DEPENDENT LIGHT CHAIN KINASE, NATURE 287: 233 (1980). (10.1038/287233a0) / NATURE (1980)
SHEPHERD, G.M., SIGNAL ENHANCEMENT IN DISTAL CORTICAL DENDRITES BY MEANS OF INTERACTIONS BETWEEN ACTIVE DENDRITIC SPINES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 82: 2192 (1985). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1985)
SMITH, S.J., DETECTION OF INTRACELLULAR CA-2+ TRANSIENTS IN SYMPATHETIC NEURONS USING ARSENAZO-III, NATURE 304: 350 (1983). (10.1038/304350a0) / NATURE (1983)
TURNER, R.W., CALCIUM-INDUCED LONG-TERM POTENTIATION IN THE HIPPOCAMPUS, NEUROSCIENCE 7: 1411 (1982). (10.1016/0306-4522(82)90254-8) / NEUROSCIENCE (1982)
WESTRUM, L.E., ELECTRON MICROSCOPIC STUDY OF STRATUM RADIATUM OF RAT HIPPOCAMPUS (REGIO SUPERIOR, CA 1) WITH PARTICULAR EMPHASIS ON SYNAPTOLOGY, JOURNAL OF COMPARATIVE NEUROLOGY 119: 281 (1962). (10.1002/cne.901190303) / JOURNAL OF COMPARATIVE NEUROLOGY (1962)
WIGSTROM, H, HIPPOCAMPAL LONG-TERM POTENTIATION IS INDUCED BY PAIRING SINGLE AFFERENT VOLLEYS WITH INTRACELLULARLY INJECTED DEPOLARIZING CURRENT PULSES, ACTA PHYSIOLOGICA SCANDINAVICA 126: 317 (1986). (10.1111/j.1748-1716.1986.tb07822.x) / ACTA PHYSIOLOGICA SCANDINAVICA (1986)
10.1126/science.3775372
WOOD, J.G., IMMUNOCYTOCHEMICAL LOCALIZATION OF CALMODULIN AND A HEAT-LABILE CALMODULIN-BINDING PROTEIN (CAM-BP80) IN BASAL GANGLIA OF MOUSE-BRAIN, JOURNAL OF CELL BIOLOGY 84: 66 (1980). (10.1083/jcb.84.1.66) / JOURNAL OF CELL BIOLOGY (1980)

Dates

Type	When
Created	18 years, 11 months ago (Oct. 5, 2006, 4:28 p.m.)
Deposited	1 year, 7 months ago (Jan. 13, 2024, 9:59 p.m.)
Indexed	1 day, 14 hours ago (Sept. 4, 2025, 10:06 a.m.)
Issued	38 years, 3 months ago (June 5, 1987)
Published	38 years, 3 months ago (June 5, 1987)
Published Print	38 years, 3 months ago (June 5, 1987)

Funders 0

None

BibTeX

@article{Gamble_1987, title={The Dynamics of Free Calcium in Dendritic Spines in Response to Repetitive Synaptic Input}, volume={236}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.3495885}, DOI={10.1126/science.3495885}, number={4806}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Gamble, Edward and Koch, Christof}, year={1987}, month=jun, pages={1311–1315} }

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