DOI: 10.1126/science.8066450. Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP

Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP

10.1126/science.8066450

Crossref journal-article

American Association for the Advancement of Science (AAAS)

Science (221)

Abstract

Repeated high-frequency trains of stimuli induce long-term potentiation (LTP) in the CA1 region that persists for up to 8 hours in hippocampal slices and for days in intact animals. This long time course has made LTP an attractive model for certain forms of long-term memory in the mammalian brain. A hallmark of long-term memory in the intact animal is a requirement for transcription, and thus whether the late phase of LTP (L-LTP) requires transcription was investigated here. With the use of different inhibitors, it was found in rat hippocampal slices that the induction of L-LTP [produced either by tetanic stimulation or by application of the cyclic adenosine monophosphate (cAMP) analog Sp-cAMPS (Sp-cyclic adenosine 3′,5′-monophosphorothioate)] was selectively prevented when transcription was blocked immediately after tetanization or during application of cAMP. As with behavioral memory, this requirement for transcription had a critical time window. Thus, the late phase of LTP in the CA1 region requires transcription during a critical period, perhaps because cAMP-inducible genes must be expressed during this period.

Bibliography

Nguyen, P. V., Abel, T., & Kandel, E. R. (1994). Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP. Science, 265(5175), 1104â1107.

Authors 3

Peter V. Nguyen (first)
Ted Abel (additional)
Eric R. Kandel (additional)

References 45 Referenced 698

ABRAHAM, W.C., MOL NEUROBIOL 5: 297 (1992). / MOL NEUROBIOL (1992)
Agranoff B. Chemistry of Mood Motivation and Memory (1970).
ALBERINI, C.M., C/EBP IS AN IMMEDIATE-EARLY GENE REQUIRED FOR THE CONSOLIDATION OF LONG-TERM FACILITATION IN APLYSIA, CELL 76: 1099 (1994). (10.1016/0092-8674(94)90386-7) / CELL (1994)
10.1038/266736a0
BAILEY, C.H., STRUCTURAL-CHANGES ACCOMPANYING MEMORY STORAGE, ANNUAL REVIEW OF PHYSIOLOGY 55: 397 (1993). (10.1146/annurev.ph.55.030193.002145) / ANNUAL REVIEW OF PHYSIOLOGY (1993)
10.1038/346724a0
10.1113/jphysiol.1973.sp010273
BLISS, T. V. P., JOURNAL OF PHYSIOLOGY-LONDON 232: 357 (1973). (10.1113/jphysiol.1973.sp010274) / JOURNAL OF PHYSIOLOGY-LONDON (1973)
BUTT, E, INHIBITION OF CGMP-DEPENDENT PROTEIN-KINASE BY (RP)-GUANOSINE 3',5'-MONOPHOSPHOROTHIOATES, FEBS LETTERS 263: 47 (1990). (10.1016/0014-5793(90)80702-K) / FEBS LETTERS (1990)
10.1016/0896-6273(88)90080-3
CHETKOVICH, D.M., NMDA RECEPTOR ACTIVATION INCREASES CYCLIC-AMP IN AREA CA1 OF THE HIPPOCAMPUS VIA CALCIUM-CALMODULIN STIMULATION OF ADENYLYL-CYCLASE, JOURNAL OF NEUROCHEMISTRY 61: 1933 (1993). (10.1111/j.1471-4159.1993.tb09836.x) / JOURNAL OF NEUROCHEMISTRY (1993)
CHETKOVICH, D.M., N-METHYL-D-ASPARTATE RECEPTOR ACTIVATION INCREASES CAMP LEVELS AND VOLTAGE-GATED CA2+ CHANNEL ACTIVITY IN AREA CA1 OF HIPPOCAMPUS, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 6467 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
COLE, A.J., RAPID INCREASE OF AN IMMEDIATE EARLY GENE MESSENGER-RNA IN HIPPOCAMPAL-NEURONS BY SYNAPTIC NMDA RECEPTOR ACTIVATION, NATURE 340: 474 (1989). (10.1038/340474a0) / NATURE (1989)
10.1038/345718a0
DASH, P.K., CAMP RESPONSE ELEMENT-BINDING PROTEIN IS ACTIVATED BY CA2+/CALMODULIN-DEPENDENT AS WELL AS CAMP-DEPENDENT PROTEIN-KINASE, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 88: 5061 (1991). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1991)
DOUGLAS, R.M., LONG-TERM POTENTIATION OF PERFORANT PATH-GRANULE CELL SYNAPSE IN RAT HIPPOCAMPUS, BRAIN RESEARCH 86: 205 (1975). (10.1016/0006-8993(75)90697-6) / BRAIN RESEARCH (1975)
DRAGUNOW, M, LONG-TERM POTENTIATION AND THE INDUCTION OF C-FOS MESSENGER-RNA AND PROTEINS IN THE DENTATE GYRUS OF UNANESTHETIZED RATS, NEUROSCIENCE LETTERS 101: 274 (1989). (10.1016/0304-3940(89)90545-4) / NEUROSCIENCE LETTERS (1989)
FREY, U, ANISOMYCIN, AN INHIBITOR OF PROTEIN-SYNTHESIS, BLOCKS LATE PHASES OF LTP PHENOMENA IN THE HIPPOCAMPAL CA1 REGION INVITRO, BRAIN RESEARCH 452: 57 (1988). (10.1016/0006-8993(88)90008-X) / BRAIN RESEARCH (1988)
10.1126/science.8389057
FREY, U, SOC NEUR ABSTR 19: 912 (1993). / SOC NEUR ABSTR (1993)
GOELET, P, THE LONG AND THE SHORT OF LONG-TERM-MEMORY - A MOLECULAR FRAMEWORK, NATURE 322: 419 (1986). (10.1038/322419a0) / NATURE (1986)
HAWKINS, R.D., LEARNING TO MODULATE TRANSMITTER RELEASE - THEMES AND VARIATIONS IN SYNAPTIC PLASTICITY, ANNUAL REVIEW OF NEUROSCIENCE 16: 625 (1993). (10.1146/annurev.ne.16.030193.003205) / ANNUAL REVIEW OF NEUROSCIENCE (1993)
HUANG, Y.Y., LEARN MEMORY 1: 74 (1994). (10.1101/lm.1.1.74) / LEARN MEMORY (1994)
HURWITZ, J, ROLE OF DEOXYRIBONUCLEIC ACID IN RIBONUCLEIC ACID SYNTHESIS, .3. INHIBITION OF ENZYMATIC SYNTHESIS OF RIBONUCLEIC ACID AND DEOXYRIBONUCLEIC ACID BY ACTINOMYCIN D AND PROFLAVIN, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 48: 1222 (1962). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1962)
JEFFERY, K.J., INDUCTION OF FOS-LIKE IMMUNOREACTIVITY AND THE MAINTENANCE OF LONG-TERM POTENTIATION IN THE DENTATE GYRUS OF UNANESTHETIZED RATS, MOLECULAR BRAIN RESEARCH 8: 267 (1990). (10.1016/0169-328X(90)90039-G) / MOLECULAR BRAIN RESEARCH (1990)
10.1038/305719a0
10.1038/266737a0
10.1126/science.2845577
10.1038/357134a0
MALINOW, R, PRESYNAPTIC ENHANCEMENT SHOWN BY WHOLE-CELL RECORDINGS OF LONG-TERM POTENTIATION IN HIPPOCAMPAL SLICES, NATURE 346: 177 (1990). (10.1038/346177a0) / NATURE (1990)
MATTHIES, H, IN SEARCH OF CELLULAR MECHANISMS OF MEMORY, PROGRESS IN NEUROBIOLOGY 32: 277 (1989). (10.1016/0301-0082(89)90024-5) / PROGRESS IN NEUROBIOLOGY (1989)
10.1016/0896-6273(91)90375-A
10.1073/pnas.88.24.11285
OTANI, S, MAINTENANCE OF LONG-TERM POTENTIATION IN RAT DENTATE GYRUS REQUIRES PROTEIN-SYNTHESIS BUT NOT MESSENGER-RNA SYNTHESIS IMMEDIATELY POST-TETANIZATION, NEUROSCIENCE 28: 519 (1989). (10.1016/0306-4522(89)90001-8) / NEUROSCIENCE (1989)
10.1038/361453a0
10.1126/science.1871602
REICH, E, ACTION OF ACTINOMYCIN DON ANIMAL CELLS AND VIRUSES, PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 48: 1238 (1962). / PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (1962)
10.1126/science.134.3478.556
10.1126/science.1720572
10.1016/0896-6273(90)90115-V
Sobell, H. M., Progress in Nucleic Acid Research and Molecular Biology 13: 153 (1973). (10.1016/S0079-6603(08)60103-8) / Progress in Nucleic Acid Research and Molecular Biology (1973)
STEWARD, O, GETTING THE MESSAGE FROM THE GENE TO THE SYNAPSE - SORTING AND INTRACELLULAR-TRANSPORT OF RNA IN NEURONS, TRENDS IN NEUROSCIENCES 15: 180 (1992). (10.1016/0166-2236(92)90170-D) / TRENDS IN NEUROSCIENCES (1992)
TAMM, I, ADV VIRUS RES 22: 187 (1978). (10.1016/S0065-3527(08)60775-7) / ADV VIRUS RES (1978)
TEYLER, T. J., BRAIN RESEARCH REVIEWS 7: 15 (1984). (10.1016/0165-0173(84)90027-4) / BRAIN RESEARCH REVIEWS (1984)
WORLEY, P.F., THRESHOLDS FOR SYNAPTIC ACTIVATION OF TRANSCRIPTION FACTORS IN HIPPOCAMPUS - CORRELATION WITH LONG-TERM ENHANCEMENT, JOURNAL OF NEUROSCIENCE 13: 4776 (1993). (10.1523/JNEUROSCI.13-11-04776.1993) / JOURNAL OF NEUROSCIENCE (1993)

Dates

Type	When
Created	18 years, 10 months ago (Oct. 5, 2006, 8:01 p.m.)
Deposited	1 year, 7 months ago (Jan. 14, 2024, 11:02 p.m.)
Indexed	1 month ago (July 27, 2025, 3:13 a.m.)
Issued	31 years ago (Aug. 19, 1994)
Published	31 years ago (Aug. 19, 1994)
Published Print	31 years ago (Aug. 19, 1994)

Funders 0

None

BibTeX

@article{Nguyen_1994, title={Requirement of a Critical Period of Transcription for Induction of a Late Phase of LTP}, volume={265}, ISSN={1095-9203}, url={http://dx.doi.org/10.1126/science.8066450}, DOI={10.1126/science.8066450}, number={5175}, journal={Science}, publisher={American Association for the Advancement of Science (AAAS)}, author={Nguyen, Peter V. and Abel, Ted and Kandel, Eric R.}, year={1994}, month=aug, pages={1104–1107} }

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