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The Journal of Neurophysiology Vol. 87 No. 6 June 2002, pp. 2770-2777
Copyright ©2002 by the American Physiological Society
1Department of Biology and 2Neuroscience Graduate Group, University of Pennsylvania, Philadelphia, PA 19104-6018; Departments of 3Physiology and 4Psychiatry, and 5Centre for Neuroscience, University of Alberta School of Medicine, Edmonton, Alberta T6G 2H7, Canada
Scharf, Matthew T.,
Newton H. Woo,
K. Matthew Lattal,
Jennie Z. Young,
Peter V. Nguyen, and
Ted Abel.
Protein Synthesis Is Required for the Enhancement of Long-Term
Potentiation and Long-Term Memory by Spaced Training. J. Neurophysiol. 87: 2770-2777, 2002. Spaced
training is generally more effective than massed training for learning
and memory, but the molecular mechanisms underlying this trial spacing
effect remain poorly characterized. One potential molecular basis for
the trial spacing effect is the differential modulation, by distinct
temporal patterns of neuronal activity, of protein synthesis-dependent
processes that contribute to the expression of specific forms of
synaptic plasticity in the mammalian brain. Long-term potentiation
(LTP) is a type of synaptic modification that may be important for
certain forms of memory storage in the mammalian brain. To explore the
role of protein synthesis in the trial spacing effect, we assessed the
protein synthesis dependence of hippocampal LTP induced by 100-Hz
tetraburst stimulation delivered to mouse hippocampal slices in either
a temporally massed (20-s interburst interval) or spaced (5-min
interburst interval) fashion. To extend our studies to the behavioral
level, we trained mice in fear conditioning using either a massed or
spaced training protocol and examined the sensitivity of long-term
memory to protein synthesis inhibition. Larger LTP was induced by
spaced stimulation in hippocampal slices. This improvement of synaptic
potentiation following temporally spaced synaptic stimulation in slices
was attenuated by bath application of an inhibitor of protein
synthesis. Further, the maintenance of LTP induced by spaced synaptic
stimulation was more sensitive to disruption by anisomycin than the
maintenance of LTP elicited following massed stimulation. Temporally
spaced behavioral training improved long-term memory for contextual but not for cued fear conditioning, and this enhancement of memory for
contextual fear was also protein synthesis dependent. Our data reveal
that altering the temporal spacing of synaptic stimulation and
behavioral training improved hippocampal LTP and enhanced contextual
long-term memory. From a broad perspective, these results suggest that
the recruitment of protein synthesis-dependent processes important for
long-term memory and for long-lasting forms of LTP can be modulated by
the temporal profiles of behavioral training and synaptic stimulation.
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