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Cited by 173Memory and Neural MechanismsSleep and Wakefulness ResearchNeural dynamics and brain function

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Hippocampal Sharp Wave/Ripples during Sleep for Consolidation of Associative Memory

Open access
Ramadan, Wiâm, Eschenko, Oxana, Sara, Susan J.·2009·PLoS ONE
DOI 10.1371/journal.pone.0006697PMC PMC2725314
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Abstract

The beneficial effect of sleep on memory has been well-established by extensive research on humans, but the neurophysiological mechanisms remain a matter of speculation. This study addresses the hypothesis that the fast oscillations known as ripples recorded in the CA1 region of the hippocampus during slow wave sleep (SWS) may provide a physiological substrate for long term memory consolidation. We trained rats in a spatial discrimination task to retrieve palatable reward in three fixed locations. Hippocampal local field potentials and cortical EEG were recorded for 2 h after each daily training session. There was an increase in ripple density during SWS after early training sessions, in both trained rats and in rats randomly rewarded for exploring the maze. In rats learning the place -reward association, there was a striking further significant increase in ripple density correlated with subsequent improvements in behavioral performance as the rat learned the spatial discrimination aspect of the task. The results corroborate others showing an experience-dependent increase in ripple activity and associated ensemble replay after exploratory activity, but in addition, for the first time, reveal a clear further increase in ripple activity related to associative learning based on spatial discrimination.

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Crossref · 10.1371/journal.pone.0006697

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Figures

Figure 1 Detection and quantification of CA1 SPW-associated ripples. A: trace 1 - local field potentials recorded at the CA1 pyramidal cell layer (1–500 Hz); trace 2 - trace 1 filtered to 150–250 Hz; traces 3 – ripple troughs; trace 4 - ripple peaks; trace 5 – ripple on/off sets; trace 6 – root mean square of trace 2. B: Illustration of the ripple detection algorithm and estimation of the ripple intrinsic properties. The ripple indicated with an asterisk on panel A is enlarged. Vertical lines indicate the ripple duration (100 ms); horizontal dotted line indicates the ripple on/off set threshold; the filled region indicates the area used to estimate the ripple magnitude. The amplitude scale is 1 mV for trace 1; 0.1 mV for trace 2; 0.05 mV for trace 6.
Figure 1 Detection and quantification of CA1 SPW-associated ripples. A: trace 1 - local field potentials recorded at the CA1 pyramidal cell layer (1–500 Hz); trace 2 - trace 1 filtered to 150–250 Hz; traces 3 – ripple troughs; trace 4 - ripple peaks; trace 5 – ripple on/off sets; trace 6 – root mean square of trace 2. B: Illustration of the ripple detection algorithm and estimation of the ripple intrinsic properties. The ripple indicated with an asterisk on panel A is enlarged. Vertical lines indicate the ripple duration (100 ms); horizontal dotted line indicates the ripple on/off set threshold; the filled region indicates the area used to estimate the ripple magnitude. The amplitude scale is 1 mV for trace 1; 0.1 mV for trace 2; 0.05 mV for trace 6.CC BY · PubMed Central
Figure 2 Performance accuracy in the spatial discrimination task, in terms of mean errors from 5 trials of a single session. The rat was allowed a maximum of 3 min to recover rewards from fixed locations. When all 3 rewarded arms were visited, the trial was terminated. Intertrial interval: 3 min. There was a significant decrease in errors over the daily sessions. *p<.05; **p<.01 (significant difference between each day and day 1); Values are means±SEM.
Figure 2 Performance accuracy in the spatial discrimination task, in terms of mean errors from 5 trials of a single session. The rat was allowed a maximum of 3 min to recover rewards from fixed locations. When all 3 rewarded arms were visited, the trial was terminated. Intertrial interval: 3 min. There was a significant decrease in errors over the daily sessions. *p<.05; **p<.01 (significant difference between each day and day 1); Values are means±SEM.CC BY · PubMed Central
Figure 3 Duration of wakefulness or SWS episodes among the three treatment groups. A. Percent time spent in wakefulness (A) or SWS (B) during the 2 h recording after daily sessions in the three groups (see Methods for the treatment of each of the groups). There were no differences on either of these measures.
Figure 3 Duration of wakefulness or SWS episodes among the three treatment groups. A. Percent time spent in wakefulness (A) or SWS (B) during the 2 h recording after daily sessions in the three groups (see Methods for the treatment of each of the groups). There were no differences on either of these measures.CC BY · PubMed Central
Figure 4 Ripple density (Ripples/min; normalized to % baseline) during the first hour of sleep after each daily session of training. Note the stable baseline in control animals receiving no training manipulation. Both “Pseudo-trained yoked rats” and “trained rats” showed a marked increase in ripple density after to the first session of training, maintained for three subsequent post training sessions. Post session ripple density in the pseudo-trained group returns to baseline by the 5th session, while in the trained group there is a significant increase in ripple density after training session 5, maintained for two subsequent sessions, returning to baseline by session 8. £: Trained vs. Control; #: Pseudo-Trained vs. Control; §trained vs. Pseudo-Trained. *p<0.05; **p<0.01. Values are means±1 SEM.
Figure 4 Ripple density (Ripples/min; normalized to % baseline) during the first hour of sleep after each daily session of training. Note the stable baseline in control animals receiving no training manipulation. Both “Pseudo-trained yoked rats” and “trained rats” showed a marked increase in ripple density after to the first session of training, maintained for three subsequent post training sessions. Post session ripple density in the pseudo-trained group returns to baseline by the 5th session, while in the trained group there is a significant increase in ripple density after training session 5, maintained for two subsequent sessions, returning to baseline by session 8. £: Trained vs. Control; #: Pseudo-Trained vs. Control; §trained vs. Pseudo-Trained. *p<0.05; **p<0.01. Values are means±1 SEM.CC BY · PubMed Central
Figure 5 Maximum post learning ripple density, plotted as a function of error score. A. on the session following the peak ripple density. (Days 6 and 7 (n = 6) or day 7 and 8 (n = 4). B. on the following day. There was a significant correlation between ripple density (ripples/min) and the behavioural performance the following day in both A and B (p = .028 and p = .05, respectively). C. Ripple density on day 9 of training as a function of error score on day 10, when most rats had learned the task. Values are means±1 SEM.
Figure 5 Maximum post learning ripple density, plotted as a function of error score. A. on the session following the peak ripple density. (Days 6 and 7 (n = 6) or day 7 and 8 (n = 4). B. on the following day. There was a significant correlation between ripple density (ripples/min) and the behavioural performance the following day in both A and B (p = .028 and p = .05, respectively). C. Ripple density on day 9 of training as a function of error score on day 10, when most rats had learned the task. Values are means±1 SEM.CC BY · PubMed Central
Figure 6 Delta power as a function of ripple density. A: Delta RMS as a function of ripple density in the trained group with data points plotted for the ten daily sessions. B: Delta RMS as a function of ripple density in the trained group during the post training session showing the highest ripple density (see Fig. 5 for determination of the sessions). The data are normalized as a percent of the baseline values recorded before training (see Methods). Note that ripple density does not vary as a function of the power of delta either overall (Fig. 5A) or on trials when there is a significant increase in ripple density. (Fig. 5B).
Figure 6 Delta power as a function of ripple density. A: Delta RMS as a function of ripple density in the trained group with data points plotted for the ten daily sessions. B: Delta RMS as a function of ripple density in the trained group during the post training session showing the highest ripple density (see Fig. 5 for determination of the sessions). The data are normalized as a percent of the baseline values recorded before training (see Methods). Note that ripple density does not vary as a function of the power of delta either overall (Fig. 5A) or on trials when there is a significant increase in ripple density. (Fig. 5B).CC BY · PubMed Central
Figure 7 Ripple magnitude (power) normalized to baseline. There is a tendency for an overall decrease in ripple magnitude over time in the control group; while both the trained and pseudo-trained group show an initial increase, then a gradual decline, the trained group remains significantly higher through session 8. *(p<0.5) and **(p<0.01): significantly different from control. Values are means±1 SEM.
Figure 7 Ripple magnitude (power) normalized to baseline. There is a tendency for an overall decrease in ripple magnitude over time in the control group; while both the trained and pseudo-trained group show an initial increase, then a gradual decline, the trained group remains significantly higher through session 8. *(p<0.5) and **(p<0.01): significantly different from control. Values are means±1 SEM.CC BY · PubMed Central

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Metadata

Authors
Ramadan, W., Eschenko, O., & Sara, S. J.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Sara, Susan J.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2009-08-20
Volume
4
Issue
8
Pages
e6697
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0006697
PMC
PMC2725314
OpenAlex
W2008915709
Cited by
173
References
44
Citations by year
2026: 6 · 2025: 8 · 2024: 10 · 2023: 3 · 2022: 9 · 2021: 4 · 2020: 13 · 2019: 16 · 2018: 12 · 2017: 14 · 2016: 10 · 2015: 10 · 2014: 12 · 2013: 14 · 2012: 6
FWCI
5.02
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Max Planck Institute for Plasma Physics (submittedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
hippocampal ripples, sharp-wave ripples, slow-wave sleep, memory consolidation, associative memory, spatial discrimination learning, sleep-dependent memory
MeSH terms
Animals, Behavior, Animal, Electroencephalography, Hippocampus, Male, Memory, Sleep, Rats, Sprague-Dawley, Rats

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